Skip to content
naulon
Get started

No retraction, correction or concern found when last checked on Oct 20, 2026.

Disease Resistance Gene Analogs (RGAs) in Plants

Manoj Sekhwal, Pingchuan Li, Irene Lam and 3 more

International Journal of Molecular Sciences · 2015 · Review · CC BY

doi:10.3390/ijms160819248

Abstract

Plants have developed effective mechanisms to recognize and respond to infections caused by pathogens. Plant resistance gene analogs (RGAs), as resistance (R) gene candidates, have conserved domains and motifs that play specific roles in pathogens’ resistance. Well-known RGAs are nucleotide binding site leucine rich repeats, receptor like kinases, and receptor like proteins. Others include pentatricopeptide repeats and apoplastic peroxidases. RGAs can be detected using bioinformatics tools based on their conserved structural features. Thousands of RGAs have been identified from sequenced plant genomes. High-density genome-wide RGA genetic maps are useful for designing diagnostic markers and identifying quantitative trait loci (QTL) or markers associated with plant disease resistance. This review focuses on recent advances in structures and mechanisms of RGAs, and their identification from sequenced genomes using bioinformatics tools. Applications in enhancing fine mapping and cloning of plant disease resistance genes are also discussed.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 20, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

Many plant-pathogen interactions are determined by the presence of resistance (R) genes/alleles that enable plants to recognize pathogens and activate inducible defenses. Plant diseases have been reported to be caused by a wide variety of pathogens, such as Fusarium sp. in fusarium head blight (FHB), Sitodiplosis mosellana in wheat midge, Blumeria sp., Erysiphe Golovinomyces sp. and Oidium in powdery mildew, Puccinia sp. in rust, Phytophthora infestans in late blight, and Pseudomonas syringae in bacterial speck. Plants have developed effective mechanisms to recognize and respond to infections with race non-specific resistance (quantitative) and race-specific resistance (qualitative). Race non-specific resistance involves a number of minor genes that are effective against several pathogens. For example, NDR1 and three alleles of rp1, rp1-D21, rp1-MD19 and rp-NC3, have been shown to confer a race non-specific resistance response to rust. In contrast, race-specific resistance is conferred by a single or a few major genes that operate in a gene-for-gene fashion in which plant R-genes recognize corresponding pathogen avirulence (Avr)-gene effectors to trigger plant defense responses. Pto in tomato confers race-specific resistance to Pseudomonas syringae pv. tomato (Pst), similarly to RPS2 in Arabidopsis and N (mosaic virus resistance gene) in tobacco. On the other hand, the wheat stem rust resistance gene Sr26 shows resistance to all races of the pathogen Puccinia graminis f. sp. tritici, thus constituting a race non-specific pathosystem.

In the defense system of plants, direct and indirect interactions are two alternative mechanisms to explain the gene-for-gene model. In the direct interaction, pathogen Avr effectors associate directly with plant R-genes to trigger signaling. For example, rice R-gene Pi-ta was shown to directly interact with Avr-Pita from Magnaporthe grisea. Likewise, a direct interaction was observed between L genes (a group of resistant genes to flax rust) and their corresponding rust Avr genes in flax. The indirect model is also known as the guard hypothesis. In this model, R-gene products act as a “guardee” to monitor the modification of host proteins after associating with the pathogenic effectors, resulting in the initiation of resistance. Examples of guardee proteins are RPM1 interacting 4 (RIN4), flagellin-sensitive 2 (FLS2), Xa21, resistance to pseudomonas syringae 5 (RPS5) and avrPphB susceptible 1 (PBS1). Resistance gene analogs (RGAs) are a large class of potential R-genes that have conserved domains and structural features. As such, RGAs can be identified from sequenced genomes using bioinformatics approaches. In the last 15 years, more than 50 plant genomes have been sequenced and assembled. Despite this great resource, only a relatively small number of R-genes have been cloned and fully characterized (Table 1) providing not only information on their structure, function and evolution, but also generating useful genetic resources to create novel resistant cultivars. In comparison, thousands of RGAs have been identified in many plant genomes (Table 2).

Though a large number of resistance gene loci have been identified in plants using linkage mapping or association studies, most of them correspond to flanking molecular markers or quantitative trait loci (QTL). Mapped genome-wide RGAs, as R-gene candidates, are valuable genomic resources to develop high-density R-gene genetic maps, design diagnostic markers and co-localize QTL. The markers designed from RGAs can be used for fine mapping and cloning of R-genes and, for breeding purposes. This review focuses on recent advances in studies of the structures and functions of RGAs, their identification using bioinformatics tools and their applications in genetic research and breeding for disease resistance.

2. Structure and Functional Mechanisms of Resistance Gene Analogs (RGA)

RGAs can be grouped as either nucleotide binding site leucine rich repeat (NBS-LRR) or transmembrane leucine rich repeat (TM-LRR). Recent findings have identified other modes of plant resistance mechanisms including pentatricopeptide repeats (PPRs) and peroxidases. NBS-LRR can be further classified as toll/interleukin receptor (TIR)-NBS-LRR (TNL) or non-TNL/coiled coil-NBS-LRR (CNL). Both TNL and CNL specifically target pathogenic effector proteins inside the host cell, termed effector triggered immunity (ETI) response. Likewise, TM-LRRs can be subdivided into two classes: receptor like kinases (RLKs) and other receptor like proteins (RLPs). RLPs and RLKs are pattern recognition receptors (PRRs) that mediate pathogen/microbe associated molecular pattern (PAMP/MAMP) triggered immunity (PTI/MTI) to allow recognition of a broad range of pathogens. PAMP/MAMPs are conserved features of most pathogens, such as chitin, flagella, and lipopolysaccharides.

2.1. Nucleotide Binding Site Leucine Rich Repeat (NBS-LRR) Family

NBS-LRR is the best-known family of RGAs. The two classes of NBS-LRR are distinguished by their N terminal TIR or non-TIR domains. The non-TIR domains are most commonly coiled coil (CC) structures. Another non-TIR domain is the leucine zipper (LZ), with interspersed hydrophobic heptad repeat sequences L-X(6)-L-X(6)-L-X(6)-L. The domain combination refers to LZ-NBS-LRR proteins which are not as common but have been found in agricultural plants such as tomato and potato. At the N-terminal region lies the highly irregular and variable LRR domain. This domain is responsible for protein-protein interactions. Between the NBS and LRR domains exists a region called the ARC domain, named so because of its occurrence in APAF-1, R protein and CED-4. This ARC domain can be further divided into ARC1 and ARC2 subdomains. The ARC domain, together with the NBS domain, forms a region for nucleotide binding.

Various conserved motifs exist within domains and subdomains of TNL and CNL. The pentapeptide EDVID (EDxxD) motif, denoted as CCD, can be identified in the CC domain. Motifs like CCR (resembling RPW8 protein) can also be found. Similarly, the TIR domains are composed of four motifs: TIR1, TIR2, TIR3 and TIR4. The NBS domain itself comprises motifs that mainly interact with nucleotides, such as the P-loop (also known as Walker A and Kinase-1a), resistance nucleotide binding site-A (RNBS-A), Walker B (Kinase-3a) and RNBS-C. The hhGRExE motif is a linker region attaching the NBS domain to the CC or TIR domains. There are two motifs on ARC1, namely GLPL (also called GxP) and Motif VII; both partake in nucleotide binding. Motifs identified in ARC2 are Motif VIII, RNBS-D, Motif X and MHD. RNBS-D motif is not consistently present between the TIR and CC domains. It likely co-evolved with their N terminal domain to allow interaction with ARC2. Figure 1 illustrates the various motifs and their structural organization in some of the most common R proteins.

NBS-LRR proteins are part of the STAND super family with ATPase activity. In the resting or auto-inhibited state, NB-ARC interacts with both its N-terminal LRR and C-terminal CC/TIR domains to maintain a closed conformation. In order to become activated, the LRR domain must be detached from the NBS domain. After detachment, the NB-ARC domain will switch its ADP nucleotides to an ATP to enable rotations within the NB-ARC domain leading to an open conformation allowing the NBS or the N-terminal regions to be exposed for subsequent downstream signaling.

As previously mentioned, TNL and CNL proteins recognize pathogen effectors that are secreted into the cell allowing plants to trigger the ETI response. Mechanisms associated with several characterized R proteins and their related ETI responses are summarized in Figure 2. Host protein RIN4 (RPM1-interacting protein 4), guarded by the NBS-LRR encoded proteins RPM1 and RPS2, is targeted by effectors such as AvrRpm1, AvrB and AvrRpt2. Similarly, enhanced disease susceptibility 1 (EDS1) is also a common target due to its ability to interact with different NBS-LRR proteins such as resistance to pseudomonas syringae 4 (RPS4), resistance to pseudomonas syringae 6 (RPS6) and suppressor of npr1-1, constitutive 1 (SNC1) during their subsequent ETI downstream response. Aside from targeting immune regulatory components, effectors can also target PTI/MTI signaling cascades (Figure 2). MAP kinase cascade, specifically MPK4, is capable of suppressing NBS-LRR protein SUMM2 in absence of effector HopAl1; however, when MPK4’s activity is compromised by HopAl1 effector, SUMM2 is activated and initiates hypersensitive programmed cell death (PCD). ETI and PTI/MTI responses usually result in the production of calcium and phytohormones, oxidative reactive oxygen species (ROS) burst, activation of MAPK cascade (s) and transcription of defense genes to facilitate the hypersensitive response (HR) in order to limit pathogen expansion. Overlaps between the ETI and PTI/MTI defense pathways exist and are important for immune regulation. However, ETI responses have a more heightened downstream effect than PTI/MTI and may also induce PTI/MTI activation in the presence of effectors. This is crucial because effector presence is a true indication of bacterial inhabitancy whereas PAMP/MAMP recognition in PTI/MTI must discriminate between harmful pathogens and beneficial microorganisms.

2.2. Receptor Like Kinase (RLK) and Receptor Like Protein (RLP) Families

RLK and RLP are main components of the first line of plant immune response triggered by microbial elicitors PAMPs or MAMPs, where the interactions between receptor and elicitor usually take place in the extracellular space. The two proteins are structurally similar with (1) a signal peptide (SP) at the beginning of N-terminus; (2) extracellular domains for perception of the microbial pattern through the leucine-rich repeats and (3) a transmembrane helix domain that can anchor RLP and RLK in the plasma membrane. RLPs differ from RLKs by the lack of an intracellular kinase domain; thus RLPs are unable to independently transduce the perceived signal into a downstream cascade. Both RLPs and RLKs are considered PRRs that recognize elicitors such as lipids, proteins, nucleic acids, and carbohydrates.

2.2.1. RLK Family

On the cell surface, plant receptors sense invasion of pathogens and transduce this information through activated signaling pathways to trigger innate immune responses. RLKs are involved in plant development and defense. In plants, serine/threonine protein kinases (STKs) can phosphorylate serine and threonine residues; receptor histidine kinases (RHKs) can phosphorylate histidine residues, e.g., ethylene (ETR1) and cytokinin receptors (CRE1). TGF β family members represent the only known STK members present in animals.

The most well-known RLKs are flagellin sensitive 2 (FLS2) and BAK1 that initiate the MAP kinase cascade upon flg22 recognition. Xa21 in rice encodes an RLK involved in resistance to a bacterial disease caused by Xanthomonas oryzae (Xoo). Several Xa21 binding proteins have been characterized; however, early events governing Xa21 signaling have not been fully elucidated. XIK1 is an RLK gene whose expression is induced rapidly upon infection with Xoo. The reduced expression of XIK1 compromised disease resistance mediated by Xa21. Xa21 binds to a WRKY transcription factor OsWRKY62. In transgenic plants, the OsWRKY62.1 variant of OsWRKY62 is overexpressed in basal defense and in Xa21-mediated resistance to Xoo. Therefore, OsWRKY62 function was implied to be a negative regulator of innate immunity in rice, which served as a critical mediator of both basal and race-specific defense responses.

2.2.2. RLP Family

Following RLKs, RLPs are the second most abundant RGAs. RLPs have a gene structure similar to RLKs but without a kinase domain (Figure 1). Of note, not all RLPs are involved in disease resistance, some play a role in plant development.

Cf-9, the first RLP gene identified, provides resistance against leaf mold induced by the fungus C. fulvum. Several Cf genes belonging to the RLP family have been isolated from tomato. Further studies revealed that Cf-9 functions in the cytoplasm by interacting with STK kinase ACIK1 via the CITRX ligand. Cf-4, a similar type of RLP, is induced by Avr4 which is an effector that protects chitinous fungi in tomato. This trigger initiates downstream PTI responses via a MAP kinase cascade, ROS accumulation and by releasing calcium ions from the vacuole (Figure 2). Another type of RLP gene, CEBiP isolated in rice, has no typical N-terminal LRR receptor for the perception of elicitor; however, two LysM motifs were observed to perceive chitin oligosaccharide patterns present in fungal cell walls, reminiscent of similar discoveries in legume. The LysM motif was also noted in the extracellular domains of two legume RLK genes, NFR1 and NFR5, and was suggested to recognize lipochitin-oligosaccharide molecules acting as a nodulation signal triggering plant organogenic processes. Thus, the LysM motifs containing PRRs were suggested to function in perception of chitin signals generated by fungi or bacteria. Additional cloned RLP genes involved in plant-pathogen resistance are listed in Table 1.

With respect to RLPs involved in plant development, two typical RLPs, CLAVATA 2 (CLV2) and too many mouths (TMM), were reported to be involved in maintaining meristematic stem cell population balance and regulating epidermis stomatal distribution in Arabidopsis, respectively. Several studies indicated that CLV2 needed to form a heterodimer with the RLK protein CLV1 via the extracellular ligand CLV3. Meanwhile, CLV2 was also required for the stabilization and accumulation of kinase CLV1. TMM was recently found to interact with both ligands, EPIDERMAL PATTERNING FACTORS (EPFs) and RLK ERECTA, to negatively regulate the development of stomata. These RLPs seemed to be irrelevant to the identification of disease resistance related RLPs. However, it was speculated that these development related genes were much more conserved than those of disease related R-genes. Based on this hypothesis, Fritz-Laylin et al. identified 73 rice disease resistance related RLP genes from a total of 90 RLPs by comparing them to their orthologs in Arabidopsis. Therefore, a better understanding of the multiple functions of RLPs and of the divergence as well as conservation between the two types of RLPs will facilitate the identification of the most interesting RLPs of this family.

2.3. Oth-R-Genes

The defense system is initiated when extracellular receptors transmit signals to their intracellular partners. To observe and receive these signals, plant cells have complex systems of TM receptors that facilitate communication between the intra- and extracellular environments. However, several reported TM receptors do not contain complete domains as observed in NBS-containing proteins, RLPs or RLKs. Thus, the term oth-R, initially proposed by Walter et al., is used to classify these peculiar RGAs. For example, RPW8.1 and RPW8.2 proteins from Arabidopsis contain a putative N-terminal TM domain and a CC domain but lack common NBS, STK or LRR domains. In response to powdery mildew infection, RPW8.2 is upregulated and trafficked to the target site, i.e., the extrahaustorial membrane, via the trans-golgi network. In contrast, RPW8.1 is involved in an assortment of pathogen-mediated responses and, as a result, may induce a broader resistance spectrum in plants. Defense gene Mlo also belongs to the TM class that has an intra- and an extracellular loop. LM1, conferring resistance to stem canker (Leptosphaeria maculans) in Brassica nigra, is predicted to have two TM motifs. Tomato Asc1 is an R-gene that provides resistance to A. alternata and, it encodes a protein with multiple TM domains and a highly conserved motif designated as the Lag1p motif. Asc1 confers insensitivity to the AAL-toxin that inhibits the enzyme sphinganine N-acyltransferase involved in sphingolipid metabolism, leading to PCD. Xa25 is a bacterial blight disease resistance gene in rice that encodes a protein of the MtN3/saliva family, which contains a region of two TM helices. Another type of Xa10 gene has been characterized in rice as a transcription activator-like (TAL) effector-dependent R-gene for resistance to bacterial blight disease. Rar1 in barley, and Rtm1, Rwm1, EDS1, NPR1, NDR1 in Arabidopsis also do not display typical LRR domains involved in pathogen recognition (Table 1).

Pti1 encodes an STK and acts downstream of Pto. It confers resistance to P. syringae in tomato, which expresses AvrPto and targets several locations in the cell (Figure 2). The immune cascade can be initiated through interaction with Pto and Prf. PBS1 can also be classified as an oth-R gene that has an STK domain and is devoid of any other known functions (; Figure 2). Fen is also a member of the STK family that mediates a hypersensitive-like response in tomato plants treated with the organophosphorous pesticide fenthion. Stpk-V, cloned from the powdery mildew resistance gene Pm21 locus, is yet another example of STK encoding genes of the Triticeae. Confocal imaging revealed the lack of bias of this protein for its subcellular localization because it was observed in membranes, cytoplasm and nuclei alike.

3. Other Defense Related Mechanisms

Aside from the typical NBS-LRR and PPR proteins involved in plant defense, recent discoveries led to the description of other modes of defense. Nomura et al. demonstrated that chloroplasts are an important component in activation and signaling of immunity. Upon exposure to flg22, chloroplast calcium-sensing receptor (CAS) dependent immune resistance and PCD are initiated. Likewise, mitochondria play a similar role, highlighting the importance of these organelles in the defense pathways activated in response to pathogen attacks.

Chloroplast and mitochondrial transmigrated proteins have been described. They belong to the PPR protein class that constitutes one of the largest protein families in plants. Intriguingly, PPR proteins have undergone an evolutionary process similar with the above-mentioned LRR associated proteins. Characteristics such as gene clustering and duplications within clusters have been observed. PPR proteins are nucleus-encoded and will translocate to the chloroplast and mitochondria to perform post transcript processing such as RNA editing, splicing and translation modification.

Known PPR genes, such as RPF2 and RPF3 in Arabidopsis, Rf1 in rice and Rf2 in maize have been identified (; Table 3). In addition, an increase in PPR1 (At1g06580) and PPR2 (At1g62720) transcripts was observed in response to pathogen attack. Although their roles were not clearly illustrated, these proteins were speculated to be involved in mitochondrial ROS metabolism. Likewise, Garcia-Andrade et al. identified a negative regulation of PPR protein chlororespiratory reduction21 (CRR21), PPRα (at4g21190) and overexpressor of cationic peroxidase3 (OCP3) in response to chitosan, a fungal PAMP/MAMP. These proteins correspond to chloroplast NADH dehydrogenase-like complex (NDH) transcript editing. NDH-mediated immune response remains inconclusive; however, ROS production and callose deposition were speculated to contribute to pathogen-mediated resistance.

As mentioned above, chloroplast and mitochondria, involved in the production of ROS, activate defense and constitutively initiate PCD. Various levels of ROS are produced at different concentrations in response to diverse pathogens. It is intriguing to note that aside from these organelles and oxidase enzymes, about half of the ROS level is generated exclusively from peroxidases upon PAMP/MAMP recognition. Apoplastic peroxidases, PRX33 and PRX34, have been well studied in response to flg22 and EF-Tu. Aside from generating hydrogen peroxide (H2O2), they play roles in callose deposition and MAMP/PAMP-mediated transcription of defense genes as well. Therefore, peroxidases are important for plant immunity.

In addition, small RNAs have been found to play a major role in defense, especially in regulating immune components in the cell; however, further studies are needed as their mechanisms remain poorly characterized.

4. Bioinformatics Approaches for RGA Identification and Characterization

To date, genome sequences of more than 50 plant species have been sequenced and assembled to various degrees; the released sequences were deposited in public databases such as Phytozome and EnsemblPlants FTP servers. Advances in next generation sequencing technologies have made whole genome sequencing one of the most important approaches in modern biological research. Current challenges include the provision of functional annotations for the large number of macromolecules. However, experimental investigations to assign protein functions are costly and time consuming. Alternatively, computational approaches to functional prediction are very attractive to solve this complex task. Mining and characterizing genome-wide plant RGAs using computational approaches are rendered possible due to their significant structural features and conserved domains. Several bioinformatics methods have been applied to identifying RGAs and predicting their functions, including sequence alignment, BLAST search, phylogenetic analysis, and domain and motif analysis using several applications such as Hidden Markov Model (HMM), SMART (http://smart.embl-heidelberg.de/), Prosite (http://prosite.expasy.org/), pfam (http://pfam.xfam.org/), and InterProScan5 (http://www.ebi.ac.uk/Tools/pfa/iprscan5/) which are summarized (Table 2 and Table 4).

Based on previously used approaches, the identification and characterization of RGAs usually follow a common procedure of four steps (Figure 3). First, a plant RGA database including all known plant RGA gene and protein sequences is generated. GenBank and PRGdb are two important sources of well curated RGA sequences. Second, BLAST searches against the RGA database are performed using a loose E-value cut-off (from 1e-5 to 1 depending on the genome size) to identify RGA candidates. Third, using the RGA candidates as input, a variety of software tools (Table 4) are employed to detect various conserved domains and motifs and produce alignments. Some programs like pfam_scan.pl (developed by Sanger) and InterproScan can be run in a parallel mode. In the last step, a dedicated sorting script is needed to group the RGA candidates into classes as per their domain and motif structures or a combination thereof. For example, to be classified as a gene encoding a TNL protein, an RGA must have a 5′ TIR and an NB-ARC followed by an LRR domain.

To date, no standardized bioinformatics tools and consistent annotation criteria were employed in individual studies. Also, individual software tools may have their own advantages and limitations in identifying different types of RGA domains. Thus, the results from different studies are not necessarily comparable. A comprehensive pipeline package to seamlessly integrate these individual tools is expected to save biologists’ time by facilitating processing, standardizing data organization and providing visualization features. The use of consistent criteria to identify the complete RGA complements would permit their comparative analyses across species.

5. Genome-Wide Identification and Characterization of RGAs

Whole genome sequencing of plants has enabled genome-wide identification, mapping and characterization of RGAs. NBS-LRR containing RGAs have been evaluated in numerous plants such as apple, Arabidopsis, barley, black cottonwood, grape, maize, Medicago, rice and sorghum (Table 2). Hundreds of NBS-LRR encoding genes have been identified from these plant genomes. NBS-LRR genes are a highly duplicated, evolutionarily diverse and clustered gene family and, they represent the major class of R-genes contributing to disease resistance in plants. Angiosperms possess NBS-LRR encoding genes but TNL encoded genes are absent from grass genomes and other monocots. It has been hypothesized that this absence is likely due to either a loss or the lack of amplification of TNL encoding genes in the monocot lineage. The loss of TNL-encoding genes in monocots could be due to increased dependence on CNL proteins. In rice, CNL proteins are encoded by many more genes than the total number of CNL and TNL genes in Arabidopsis. More NBS-LRR and CNL encoding genes have been identified in most monocots than in dicots (Table 2). CNL and TNL proteins may utilize different downstream signaling components in disease resistance responses. This genomic shift to CNL genes in monocots could have resulted from mutations in genes encoding downstream components of TNL-specific pathways, resulting in a loss of function and conservative selection for TNL genes. Therefore, TNL-encoding genes may have been lost or simply never amplified in monocot genomes due to a lack of selective advantage. In addition, some dicots like Arabidopsis contain more TNL than CNL. The abundance of TNL likely results from its older origin than CNL. Besides TNL and CNL, variants of NBS encoding genes such as CN, NL, TN and N vary largely in number (Table 2). Other NBS-LRR like domains such as CTNL and CTN in apple, TN-TNL, TTNL, XTNX and SA-CA (signalling commentator with CC domain, e.g., RPW8) in Arabidopsis, and, CNLX, CNX, CNXL, CXN, NX and NLX in sorghum, were reported. Numbers of TIR-X RGAs were also reported such as 126 in cabbages, 46 in Arabidopsis, 67 in cottonwood and 92 in Medicago.

More than 600 members of RLKs were identified in Arabidopsis and around 1200 members in rice. They have also been reported in maize, wheat, tomato and cottonwood (Table 2). RLPs with TM domain have also been reported in Arabidopsis and tomato (Table 2). Some cloned genes, such as Hs1pro-1 in sugar beet, Cf2, Cf4-9, Ve1 and Hcr9-4E in tomato, belong to this class (Table 1).

Some RGAs have been identified as pseudogenes. A total of 49 R-pseudogenes in Medicago, 179 in potato, 347 in the rice variety “Nipponbare” and 345 in variety “93-11”, 10 in Arabidopsis, 161 in cottonwood and 62 in lotus have been identified. In tomato, only 10% of the cloned RGAs were classified into pseudogenes, but almost half of the identified RGAs were pseudogenes in western white pine (Pinus monticola). Pseudogene paralogs of several R-genes such as Xa21, Cf9, Pto and Dm3, were also identified. Most identified pseudogenes have strong identity with another NBS protein but their sequences are shortened by premature stop codons or frameshift mutations. Sequence comparisons have suggested that RGA pseudogenes originated from point mutations, like insertion or deletion of nucleotides. Usually, pseudogenes are considered non-functional genes; however, some pseudogenes can be transcribed into mRNA. Evidence of expression also exists in species such as rice, pine and Medicago. In these species, some pseudogenes have 90%–100% identity to ESTs and their functions are ascribed as partial NBS-LRR proteins. Pseudogenes are believed to power R gene evolution by driving illegitimate recombination and permitting gene conversion with alleles or paralogs of functional R-genes.

As noted earlier, there is surprising similarity in the PPR genes of Arabidopsis and rice supporting their existence prior to the divergence of monocots and dicots. However, massive differences between the numbers of PPR genes in higher plants and non-plant organisms are indicative of the expansion of this gene family during the evolution of the plant kingdom.

Some RGAs represent a highly divergent defense system in plants, containing a large and diverse family of genes with conserved motifs and domains. To understand the phylogenetic relationship of RGAs, we selected 63 well-characterized RGAs or cloned R-genes (Table 1) in seven dicot (Arabidopsis, black pepper, flax, lettuce, potato, tobacco and tomato) and four monocot species (barley, maize, rice and wheat) from the NCBI database. These selected RGAs represent the major classes of RGAs: NBS-LRR (CNL, TNL or NL), RLK (LRR-STK) and RLP (LRR-TM). A neighbor-joining tree with 63 RGAs was constructed using MEGA 6 (Figure 4). RGAs were classified into two groups: Clade I for NBS-LRR encoding genes and Clade II for RLK and RLP encoding genes. As RLP and RLK proteins have common domains but differ in presence or absence of a kinase (Figure 1B), LRR-STK and LRR-TM encoding genes clustered into one large group (Clade II) with sub-clusters. CNL and TNL are major subclasses of NBS-LRR encoding genes; thus they grouped into distinct sub-clusters in Clade I (Clades Ia for TNL and Ib for CNL encoding genes, respectively) (Figure 4). We observed that TNL encoding genes were conserved among different dicot species (Clade Ia). In contrast, CNL encoding genes are much more diverse. Some of them are conserved within angiosperms (Clades Ib-2 and Ib-4), within dicots (Clades Ib-1 and Ib-3) or within monocots (Clade Ib-5), while others have diverged between dicot and monocot species (Clade Ib) or within dicots (between Clades Ib-3 and Ib-5). For example, Clade Ib-3 contains RGAs from dicot species only while Clade Ib-5, from monocot species only. In addition, NL and LZ-NL encoding genes may be more closely related to CNL than to TNL because almost all NL and LZ-NL encoding genes clustered with the CNL clades (Clades Ib-1, Ib-2, Ib-3, Ib-4 and Ib-5), suggesting that the variants of non-TNL, such as NL and LZ-NL, may have evolved from CNL rather than TNL.

6. Genome Organization of RGAs

Many studies revealed that RGAs are irregularly distributed in plant genomes and that many reside in clusters. The clustered distribution of RGAs provides a reservoir of genetic variation to drive the evolution of new R-gene specificities.

Most RGAs are found in clusters. For example, 38.2% of the mapped NBS genes were located into eight clusters in the lotus genome. Similarly, 50% and 51% of NBS genes were clustered in the rice and Brachypodium genome, respectively. Higher rates have been found in other species such as potato where 73% of the mapped NBS-LRR genes grouped into 63 clusters, while approximately 80% were clustered in Medicago, 74.3% in the rice cultivar “Nipponbare” and 71.1% and 63.8% in Arabidopsis and lyrata, respectively. Many super-clusters were identified for NBS-LRR genes, including a super-cluster with 11 NBS genes on chromosome 4 of Brachypodium and one with 82 NBS-encoded genes in Medicago. In addition, some R-genes appear in complex cluster structures forming a diverse multigene family such as Cf4/9 in tomato, L in flax, Mla in barley, Pi2/9 in rice, Dm3/13 in lettuce and I2 in tomato. The structures of three haplotypes (linked genes) of the Pto cluster in tomato have been defined while a single haplotype of the Xa21 cluster in rice was partially characterized. Several restorer genes, like the Rf gene from various plant species, showed homology to a cluster of PPR genes. Genes within a single cluster may determine resistance to different pathogens.

RGAs are often irregularly distributed on chromosomes. Gebhardt et al. and Lozano et al. published genetic maps of potato with resistance traits. Their analyses indicated that large numbers of NBS-LRR genes were found on chromosomes 4 and 11 (approximately 15% of the mapped genes), while only 1% was on chromosome 3. In Medicago, chromosomes 6 and 3 encoded approximately 34% and 40% of all TNLs, respectively. In apple, 56% of the 868 identified RGAs were distributed on six chromosomes (Chr 2, 7, 8, 10, 11 and 15) including 25% on Chr 2 while 99% of the non-TNL class was on Chr 11. Pseudogenes are also distributed and clustered at specific chromosomal locations in the same way as functional NBS-LRR genes. Pseudogenes evolve much faster than functional genes and represent a reservoir for evolution of new specificities.

In conclusion, genetic and molecular data have shown that disease resistance genes are frequently clustered in plant genomes. Several cloned R-genes have common domains which will help to identify disease resistance loci from clusters of paralogs. R loci may harbor single genes with multiple alleles, for instance, the L locus in flax with 13 alleles or RPM1 in Arabidopsis with two. However, some resistance loci and clusters of resistance genes are inherently unstable, e.g., Rp1 in maize was described as a fast evolving complex.

7.1. RGAs Are R-Gene Candidates for Disease Resistance

Map-based cloning remains the major strategy for isolating resistance genes, a strategy that requires high-density genetic maps. Genome-wide RGA identification will facilitate the development of molecular markers towards R-gene mapping and cloning. To date, all cloned disease resistance genes in plants belong to several major classes of RGAs (Table 1). Genome-wide RGAs can be interrogated as R-gene candidates. In sorted and assembled genome sequences, the physical location of the identified RGAs can be easily retrieved. Single nucleotide polymorphism (SNP) markers can be designed from RGAs around a target disease gene to construct an RGA genetic map for the specific target region. These mapped genome-wide RGAs and SNP markers in their vicinity are valuable tools to develop high density R-gene genetic maps, target R-genes, co-localize QTL, design diagnostic markers of R-genes for fine mapping and cloning of R-genes and for resistance breeding.

7.2. Genome-Wide Association Study (GWAS) with Mapped RGAs Helps Co-Localization of QTL to Resistance Genes

Linkage mapping has been a key tool to identify resistance genes in the past 30 years. However, linkage mapping is sometimes limited by population size or low frequency of recombinant events near the target genes of interest resulting in increased expense and gene cloning difficulties. Under this scenario, association mapping, an application of linkage disequilibrium (LD), was developed to address these issues. Today, modern genotyping techniques such as genotyping by sequencing (GBS) and chip-based genotyping facilitate GWAS for qualitative gene and QTL mapping. The primary advantage of GWAS over linkage mapping is the unprecedented high resolution across the whole genome. Consequently, population size for fine mapping may not need to be as large as for linkage mapping. With the aid of the identified and mapped genome-wide RGAs, more genes or QTL associated with disease resistance are able to be fine-mapped and co-localized.

Along with the development of comprehensive plant haplotype mapping projects in different crops such as Arabidopsis (http://1001genomes.org/), flax (http://tufgen.ca), rice (http://ncgr.ac.cn/ricehap3/), wheat (http://wheatgenome.org) and maize (http://panzea.org), a large number of crop varieties, ecotypes or breeding lines have been resequenced. The sequencing information of most projects has been released to the research community. These projects provide biologists with an invaluable blueprint to exploit SNP and indel markers, comparable to the prestigious human 1000 Hapmap project (http://1000genomes.org). These plant haplotype maps permit the establishment of relationships between RGAs and plant disease resistance, providing precise sequence information to design diagnostic markers for breeding and to identify R-genes.

7.3. RGA Mapping in Plants with Limited Genome Information

In addition to the traditional marker types to construct genetic linkage maps such as random amplified polymorphic DNA (RAPD), restriction fragment length polymorphism (RFLP), cleaved amplified polymorphic sequence (CAPS), amplified fragment length polymorphism (AFLP), simple sequence repeat (SSR) and SNP markers, specific methods have emerged from the identification of RGAs. NBS profiling is a useful and practical linkage map construction method based on genetic markers that has been implemented in potato. NBS profiling was first used to map RGAs in cauliflower where a genetic linkage map was constructed based on the combined use of AFLP and NBS profiling. Linden et al., have described an advanced NBS profiling approach based on conserved NBS amplification in several crop plants such as potato, tomato, barley and lettuce.

Degenerated primers have been designed to clone NBS genes according to their conserved domain structure using PCR. With a properly constructed mapping population such as a doubled haploid (DH) or a recombinant inbred line (RIL) population, an NBS linkage map can initially sort out these markers by linkage groups or chromosomes. This method is used when the whole genome has yet to be sequenced and assembled because it directly associates the markers with the target gene class. Furthermore, with proper modification of the degenerated primers design, NBS profiling can also be extended to other RGAs as long as the gene family of interest contains substantial members across all chromosomes. Therefore, although many species of interest have already been sequenced and large numbers of SNPs have been identified in these species, NBS profiling remains a powerful tool for the development of markers linked to resistance loci in species with limited genome information. A similar profiling method for other R-gene classes, like peroxidase profiling, developed in barley, revealed the resistance of R-genes for rusts and mildew. RLK and LRR profiling strategies in potato were also developed. Meanwhile, other non-RGA gene families can also benefit from this idea, like MYB profiling in pot azalea.

8. Conclusions

Plant RGAs are a large group of potential R-genes that have conserved domains and structural features which have specific roles in host-pathogen interactions. Bioinformatics software tools and comprehensive pipelines will help in their identification and characterization. Numerous RGAs have been identified from several sequenced plant genomes. These identified genome-wide RGAs with applications in genomics and bioinformatics such as linkage mapping, GWAS, clustering and protein signature profiling will assist traditional methods to enhance marker development, QTL mapping, cloning of plant resistance genes and resistance breeding.

References 282

  1. 1.

    Grant M.R., McDowell J.M., Sharpe A.G., de Torres Zabala M., Lydiate D.J., Dangl J.L. Independent deletions of a pathogen-resistance gene in Brassica and Arabidopsis. Proc. Natl. Acad. Sci. USA. 1998;95:15843-15848.

    Not in our library10.1073/pnas.95.26.15843

  2. 2.

    Buerstmayr H., Ban T., Anderson J.A. QTL mapping and marker-assisted selection for fusarium head blight resistance in wheat: A review. Plant Breed. 2009;128:1-26.

    Not in our library10.1111/j.1439-0523.2008.01550.x

  3. 3.

    Doane J.F., Olfert O., Mukerji M.K. Extraction precision of sieving and brine floatation for removal of wheat midge, Sitodiplosis mosellana (Diptera: Cecidomyiidae), cocoons and larvae from soil. J. Econ. Entomol. 1986;80:268-271.

    Not in our library10.1093/jee/80.1.268

  4. 4.

    Hacquard S., Kracher B., Maekawa T., Vernaldi S., Schulze-Lefert P., Ver Loren van Themaat E. Mosaic genome structure of the barley powdery mildew pathogen and conservation of transcriptional programs in divergent hosts. Proc. Natl. Acad. Sci. USA. 2013;110:E2219-E2228.

    Not in our library10.1073/pnas.1306807110

  5. 5.

    Hooker A.L. The genetics and expression of resistance in plants to rusts of the genus Puccinia. Annu. Rev. Phytopathol. 1967;5:163-182.

    Not in our library10.1146/annurev.py.05.090167.001115

  6. 6.

    Nowicki M., Foolad M.R., Nowakowska M., Kozik E.U. Potato and tomato late blight caused by Phytophthora infestans: An overview of pathology and resistance breeding. Plant Dis. 2012;96:4-17.

    Not in our library10.1094/pdis-05-11-0458

  7. 7.

    Preston G.M. Pseudomonas syringae pv. tomato: The right pathogen, of the right plant, at the right time. Mol. Plant Pathol. 2000;1:263-275.

    Not in our library10.1046/j.1364-3703.2000.00036.x

  8. 8.

    Burdon J.J., Barrett L.G., Rebetzke G., Thrall P.H. Guiding deployment of resistance in cereals using evolutionary principles. Evol. Appl. 2014;7:609-624.

    Not in our library10.1111/eva.12175

  9. 9.

    Hulbert S.H. Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu. Rev. Phytopathol. 1997;35:293-310.

    Not in our library10.1146/annurev.phyto.35.1.293

  10. 10.

    Van der Biezen E.A., Jones J.D. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 1998;23:454-456.

    Not in our library10.1016/s0968-0004(98)01311-5

  11. 11.

    Kobe B., Deisenhofer J. The leucine-rich repeat: A versatile binding motif. Trends Biochem. Sci. 1994;19:415-421.

    Not in our library10.1016/0968-0004(94)90090-6

  12. 12.

    McIntosh R.A., Wellings C.R., Park R.F. Wheat Rusts: An Atlas of Resistance Genes. 1995;1-204.

    Not in our library

  13. 13.

    Jia Y., McAdams S.A., Bryan G.T., Hershey H.P., Valent B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 2000;19:4004-4014.

    Not in our library10.1093/emboj/19.15.4004

  14. 14.

    Dodds P.N., Lawrence G.J., Catanzariti A.M., Teh T., Wang C.I., Ayliffe M.A., Kobe B., Ellis J.G. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA. 2006;103:8888-8893.

    Not in our library10.1073/pnas.0602577103

  15. 15.

    McDowell J.M., Woffenden B.J. Plant disease resistance genes: Recent insights and potential applications. Trends Biotechnol. 2003;21:178-183.

    Not in our library10.1016/s0167-7799(03)00053-2

  16. 16.

    Ameline-Torregrosa C., Wang B.B., O’Bleness M.S., Deshpande S., Zhu H., Roe B., Young N.D., Cannon S.B. Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol. 2008;146:5-21.

    Not in our library10.1104/pp.107.104588

  17. 17.

    Arya P., Kumar G., Acharya V., Singh A.K. Genome-wide identification and expression analysis of NBS-encoding genes in Malus x domestica and expansion of NBS genes family in Rosaceae. PLoS ONE. 2014;9:e107987.

    Not in our library10.1371/journal.pone.0107987

  18. 18.

    Dilbirligi M., Gill K.S. Identification and analysis of expressed resistance gene sequences in wheat. Plant Mol. Biol. 2003;53:771-787.

    Not in our library10.1023/b:plan.0000023663.55701.5f

  19. 19.
    The genome portal of the Department of Energy Joint Genome Institute: 2014 updates · 2013
    No notice
  20. 20.

    Goodstein D.M., Shu S., Howson R., Neupane R., Hayes R.D., Fazo J., Mitros T., Dirks W., Hellsten U., Putnam N., et al. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res. 2012;40:D1178-D1186.

    Not in our library10.1093/nar/gkr944

  21. 21.

    Monaco M.K., Stein J., Naithani S., Wei S., Dharmawardhana P., Kumari S., Amarasinghe V., Youens-Clark K., Thomason J., Preece J., et al. Gramene 2013: Comparative plant genomics resources. Nucleic Acids Res. 2014;42:D1193-D1199.

    Not in our library10.1093/nar/gkt1110

  22. 22.

    Liu J., Liu X., Dai L., Wang G. Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. J. Genet. Genom. 2007;34:765-776.

    Not in our library10.1016/s1673-8527(07)60087-3

  23. 23.

    Feuillet C., Travella S., Stein N., Albar L., Nublat A., Keller B. Map-based isolation of the leaf rust disease resistance gene Lr10 from the hexaploid wheat (Triticum aestivum L.) genome. Proc. Natl. Acad. Sci. USA. 2003;100:15253-15258.

    Not in our library10.1073/pnas.2435133100

  24. 24.

    Cloutier S., McCallum B.D., Loutre C., Banks T.W., Wicker T., Feuillet C., Keller B., Jordan M.C. Leaf rust resistance gene Lr1, isolated from bread wheat (Triticum aestivum L.) is a member of the large psr567 gene family. Plant Mol. Biol. 2007;65:93-106.

    Not in our library10.1007/s11103-007-9201-8

  25. 25.

    Yahiaoui N., Srichumpa P., Dudler R., Keller B. Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J. 2004;37:528-538.

    Not in our library10.1046/j.1365-313x.2003.01977.x

  26. 26.

    Periyannan S., Moore J., Ayliffe M., Bansal U., Wang X., Huang L., Deal K., Luo M., Kong X., Bariana H., et al. The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science. 2013;341:786-788.

    Not in our library10.1126/science.1239028

  27. 27.

    Saintenac C., Zhang W., Salcedo A., Rouse M.N., Trick H.N., Akhunov E., Dubcovsky J. Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science. 2013;341:783-786.

    Not in our library10.1126/science.1239022

  28. 28.

    Huang L., Brooks S.A., Li W., Fellers J.P., Trick H.N., Gill B.S. Map-based cloning of leaf rust resistance gene Lr21 from the large and polyploid genome of bread wheat. Genetics. 2003;164:655-664.

    Not in our library10.1093/genetics/164.2.655

  29. 29.

    Lagudah E.S., Moullet O., Appels R. Map-based cloning of a gene sequence encoding a nucleotide-binding domain and a leucine-rich region at the Cre3 nematode resistance locus of wheat. Genome. 1997;40:659-665.

    Not in our library10.1139/g97-087

  30. 30.
    The Cre1 and Cre3 Nematode Resistance Genes Are Located at Homeologous Loci in the Wheat Genome · 2003
    Not checked
  31. 31.

    Liu W., Frick M., Huel R., Nykiforuk C.L., Wang X., Gaudet D.A., Eudes F., Conner R.L., Kuzyk A., Chen Q., et al. The stripe rust resistance gene Yr10 encodes an evolutionary-conserved and unique CC-NBS-LRR sequence in wheat. Mol. Plant. 2014;7:1740-1755.

    Not in our library10.1093/mp/ssu112

  32. 32.

    Cao A., Xing L., Wang X., Yang X., Wang W., Sun Y., Qian C., Ni J., Chen Y., Liu D., et al. Serine/threonine kinase gene Stpk-V, a key member of powdery mildew resistance gene Pm21, confers powdery mildew resistance in wheat. Proc. Natl. Acad. Sci. USA. 2011;108:7727-7732.

    Not in our library10.1073/pnas.1016981108

  33. 33.

    Krattinger S.G., Lagudah E.S., Spielmeyer W., Singh R.P., Huerta-Espino J., McFadden H., Bossolini E., Selter L.L., Keller B. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323:1360-1363.

    Not in our library10.1126/science.1166453

  34. 34.

    Fu D., Uauy C., Distelfeld A., Blechl A., Epstein L., Chen X., Sela H., Fahima T., Dubcovsky J. A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science. 2009;323:1357-1360.

    Not in our library10.1126/science.1166289

  35. 35.

    Halterman D., Zhou F., Wei F., Wise R.P., Schulze-Lefert P. The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J. 2001;25:335-348.

    Not in our library10.1046/j.1365-313x.2001.00982.x

  36. 36.

    Zhou F., Kurth J., Wei F., Elliott C., Vale G., Yahiaoui N., Keller B., Somerville S., Wise R., Schulze-Lefert P. Cell-autonomous expression of barley Mla1 confers race-specific resistance to the powdery mildew fungus via a Rar1-independent signaling pathway. Plant Cell. 2001;13:337-350.

    Not in our library10.1105/tpc.13.2.337

  37. 37.

    Halterman D.A., Wei F., Wise R.P. Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames. Plant Physiol. 2003;131:558-567.

    Not in our library10.1104/pp.014407

  38. 38.

    Brueggeman R., Rostoks N., Kudrna D., Kilian A., Han F., Chen J., Druka A., Steffenson B., Kleinhofs A. The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl. Acad. Sci. USA. 2002;99:9328-9333.

    Not in our library10.1073/pnas.142284999

  39. 39.

    Buschges R., Hollricher K., Panstruga R., Simons G., Wolter M., Frijters A., van Daelen R., van der Lee T., Diergaarde P., Groenendijk J., et al. The barley Mlo gene: A novel control element of plant pathogen resistance. Cell. 1997;88:695-705.

    Not in our library10.1016/s0092-8674(00)81912-1

  40. 40.

    Salmeron J.M., Oldroyd G.E., Rommens C.M., Scofield S.R., Kim H.S., Lavelle D.T., Dahlbeck D., Staskawicz B.J. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell. 1996;86:123-133.

    Not in our library10.1016/s0092-8674(00)80083-5

  41. 41.

    Milligan S.B., Bodeau J., Yaghoobi J., Kaloshian I., Zabel P., Williamson V.M. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell. 1998;10:1307-1319.

    Not in our library10.1105/tpc.10.8.1307

  42. 42.

    Ori N., Eshed Y., Paran I., Presting G., Aviv D., Tanksley S., Zamir D., Fluhr R. The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell. 1997;9:521-532.

    Not in our library10.1105/tpc.9.4.521

  43. 43.

    Zhang C., Liu L., Wang X., Vossen J., Li G., Li T., Zheng Z., Gao J., Guo Y., Visser R.G., et al. The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to Phytophthora infestans. Theor. Appl. Genet. 2014;127:1353-1364.

    Not in our library10.1007/s00122-014-2303-1

  44. 44.

    Brommonschenkel S.H., Tanksley S.D. Map-based cloning of the tomato genomic region that spans the Sw-5 tospovirus resistance gene in tomato. Mol. Gen. Genet. 1997;256:121-126.

    Not in our library10.1007/s004380050553

  45. 45.

    Lanfermeijer F.C., Dijkhuis J., Sturre M.J., de Haan P., Hille J. Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon esculentum. Plant Mol. Biol. 2003;52:1037-1049.

    Not in our library10.1023/a:1025434519282

  46. 46.

    Schornack S., Ballvora A., Gurlebeck D., Peart J., Baulcombe D., Ganal M., Baker B., Bonas U., Lahaye T. The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J. 2004;37:46-60.

    Not in our library10.1046/j.1365-313x.2003.01937.x

  47. 47.

    Ernst K., Kumar A., Kriseleit D., Kloos D.U., Phillips M.S., Ganal M.W. The broad-spectrum potato cyst nematode resistance gene Hero from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J. 2002;31:127-136.

    Not in our library10.1046/j.1365-313x.2002.01341.x

  48. 48.

    Dixon M.S., Jones D.A., Keddie J.S., Thomas C.M., Harrison K., Jones J.D. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996;84:451-459.

    Not in our library10.1016/s0092-8674(00)81290-8

  49. 49.

    Parniske M., Hammond-Kosack K.E., Golstein C., Thomas C.M., Jones D.A., Harrison K., Wulff B.B., Jones J.D. Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato. Cell. 1997;91:821-832.

    Not in our library10.1016/s0092-8674(00)80470-5

  50. 50.

    Dixon M.S., Hatzixanthis K., Jones D.A., Harrison K., Jones J.D. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell. 1998;10:1915-1925.

    Not in our library10.1105/tpc.10.11.1915

  51. 51.

    Jones D.A., Thomas C.M., Hammond-Kosack K.E., Balint-Kurti P.J., Jones J.D. Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science. 1994;266:789-793.

    Not in our library10.1126/science.7973631

  52. 52.

    Kawchuk L.M., Hachey J., Lynch D.R., Kulcsar F., van Rooijen G., Waterer D.R., Robertson A., Kokko E., Byers R., Howard R.J., et al. Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl. Acad. Sci. USA. 2001;98:6511-6515.

    Not in our library10.1073/pnas.091114198

  53. 53.

    Martin G.B., Frary A., Wu T., Brommonschenkel S., Chunwongse J., Earle E.D., Tanksley S.D. A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death. Plant Cell. 1994;6:1543-1552.

    Not in our library10.1105/tpc.6.11.1543

  54. 54.

    Martin G.B., Brommonschenkel S.H., Chunwongse J., Frary A., Ganal M.W., Spivey R., Wu T., Earle E.D., Tanksley S.D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993;262:1432-1436.

    Not in our library10.1126/science.7902614

  55. 55.

    Zhou J., Loh Y.T., Bressan R.A., Martin G.B. The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell. 1995;83:925-935.

    Not in our library10.1016/0092-8674(95)90208-2

  56. 56.

    Bendahmane A., Kanyuka K., Baulcombe D.C. The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell. 1999;11:781-792.

    Not in our library10.1105/tpc.11.5.781

  57. 57.

    Song J., Bradeen J.M., Naess S.K., Raasch J.A., Wielgus S.M., Haberlach G.T., Kuang H., Liu J., Austin-Phillips S., Buell C.R., et al. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad. Sci. USA. 2003;100:9128-9133.

    Not in our library10.1073/pnas.1533501100

  58. 58.

    Bendahmane A., Querci M., Kanyuka K., Baulcombe D.C. Agrobacterium transient expression system as a tool for the isolation of disease resistance genes: Application to the Rx2 locus in potato. Plant J. 2000;21:73-81.

    Not in our library10.1046/j.1365-313x.2000.00654.x

  59. 59.

    Ballvora A., Ercolano M.R., Weiss J., Meksem K., Bormann C.A., Oberhagemann P., Salamini F., Gebhardt C. The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J. 2002;30:361-371.

    Not in our library10.1046/j.1365-313x.2001.01292.x

  60. 60.

    Meyers B.C., Shen K.A., Rohani P., Gaut B.S., Michelmore R.W. Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection. Plant Cell. 1998;10:1833-1846.

    Not in our library10.1105/tpc.10.11.1833

  61. 61.

    Tai T.H., Dahlbeck D., Clark E.T., Gajiwala P., Pasion R., Whalen M.C., Staskawicz B.J., Stall R.E. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl. Acad. Sci. USA. 1999;96:14153-14158.

    Not in our library10.1073/pnas.96.24.14153

  62. 62.
    Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation · 1998
    Not checked
  63. 63.

    Wang Z.X., Yano M., Yamanouchi U., Iwamoto M., Monna L., Hayasaka H., Katayose Y., Sasaki T. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 1999;19:55-64.

    Not in our library10.1046/j.1365-313x.1999.00498.x

  64. 64.

    Bryan G.T., Wu K.S., Farrall L., Jia Y., Hershey H.P., McAdams S.A., Donaldson G.K., Faulk K.N., Tarchini R., Valent B. tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell. 2000;12:2033-2046.

    Not in our library10.1105/tpc.12.11.2033

  65. 65.

    Liu X., Lin F., Wang L., Pan Q. The in silico map-based cloning of Pi36, a rice coiled-coil nucleotide-binding site leucine-rich repeat gene that confers race-specific resistance to the blast fungus. Genetics. 2007;176:2541-2549.

    Not in our library10.1534/genetics.107.075465

  66. 66.

    Okuyama Y., Kanzaki H., Abe A., Yoshida K., Tamiru M., Saitoh H., Fujibe T., Matsumura H., Shenton M., Galam D.C., et al. A multifaceted genomics approach allows the isolation of the rice Pia-blast resistance gene consisting of two adjacent NBS-LRR protein genes. Plant J. 2011;66:467-479.

    Not in our library10.1111/j.1365-313x.2011.04502.x

  67. 67.

    Sharma T.R., Madhav M.S., Singh B.K., Shanker P., Jana T.K., Dalal V., Pandit A., Singh A., Gaikwad K., Upreti H.C., et al. High-resolution mapping, cloning and molecular characterization of the Pi-kh gene of rice, which confers resistance to Magnaporthe grisea. Mol. Genet. Genom. 2005;274:569-578.

    Not in our library10.1007/s00438-005-0035-2

  68. 68.

    Lin F., Chen S., Que Z., Wang L., Liu X., Pan Q. The blast resistance gene Pi37 encodes a nucleotide binding site leucine-rich repeat protein and is a member of a resistance gene cluster on rice chromosome 1. Genetics. 2007;177:1871-1880.

    Not in our library10.1534/genetics.107.080648

  69. 69.
    The Rice Bacterial Blight Resistance Gene xa5 Encodes a Novel Form of Disease Resistance · 2004
    Not checked
  70. 70.

    Chu Z., Yuan M., Yao J., Ge X., Yuan B., Xu C., Li X., Fu B., Li Z., Bennetzen J.L., et al. Promoter mutations of an essential gene for pollen development result in disease resistance in rice. Genes Dev. 2006;20:1250-1255.

    Not in our library10.1101/gad.1416306

  71. 71.

    Das A., Soubam D., Singh P.K., Thakur S., Singh N.K., Sharma T.R. A novel blast resistance gene, Pi54rh cloned from wild species of rice, Oryza rhizomatis confers broad spectrum resistance to Magnaporthe oryzae. Funct. Integr. Genom. 2012;12:215-228.

    Not in our library10.1007/s10142-012-0284-1

  72. 72.

    Liu G., Lu G., Zeng L., Wang G.L. Two broad-spectrum blast resistance genes, Pi9(t) and Pi2(t), are physically linked on rice chromosome 6. Mol. Genet. Genom. 2002;267:472-480.

    Not in our library10.1007/s00438-002-0677-2

  73. 73.

    Zhou B., Qu S., Liu G., Dolan M., Sakai H., Lu G., Bellizzi M., Wang G.L. The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol. Plant Microbe Interact. 2006;19:1216-1228.

    Not in our library10.1094/mpmi-19-1216

  74. 74.

    Sakamoto K., Tada Y., Yokozeki Y., Akagi H., Hayashi N., Fujimura T., Ichikawa N. Chemical induction of disease resistance in rice is correlated with the expression of a gene encoding a nucleotide binding site and leucine-rich repeats. Plant Mol. Biol. 1999;40:847-855.

    Not in our library10.1023/a:1006244323934

  75. 75.

    Shang J., Tao Y., Chen X., Zou Y., Lei C., Wang J., Li X., Zhao X., Zhang M., Lu Z., et al. Identification of a new rice blast resistance gene, Pid3, by genomewide comparison of paired nucleotide-binding site-leucine-rich repeat genes and their pseudogene alleles between the two sequenced rice genomes. Genetics. 2009;182:1303-1311.

    Not in our library10.1534/genetics.109.102871

  76. 76.

    Song W.Y., Wang G.L., Chen L.L., Kim H.S., Pi L.Y., Holsten T., Gardner J., Wang B., Zhai W.X., Zhu L.H., et al. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science. 1995;270:1804-1806.

    Not in our library10.1126/science.270.5243.1804

  77. 77.

    Sun X., Cao Y., Wang S. Point mutations with positive selection were a major force during the evolution of a receptor-kinase resistance gene family of rice. Plant Physiol. 2006;140:998-1008.

    Not in our library10.1104/pp.105.073080

  78. 78.

    Kaku H., Nishizawa Y., Ishii-Minami N., Akimoto-Tomiyama C., Dohmae N., Takio K., Minami E., Shibuya N. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA. 2006;103:11086-11091.

    Not in our library10.1073/pnas.0508882103

  79. 79.

    Tian D., Wang J., Zeng X., Gu K., Qiu C., Yang X., Zhou Z., Goh M., Murata-Hori M., Luo Y., et al. The rice TAL effector-dependent resistance protein XA10 triggers cell death and calcium depletion in the endoplasmic reticulum. Plant Cell. 2014;26:497-515.

    Not in our library10.1105/tpc.113.119255

  80. 80.

    Liu Q., Yuan M., Zhou Y., Li X., Xiao J., Wang S. A paralog of the MtN3/saliva family recessively confers race-specific resistance to Xanthomonas oryzae in rice. Plant Cell Environ. 2011;34:1958-1969.

    Not in our library10.1111/j.1365-3040.2011.02391.x

  81. 81.

    Bimolata W., Kumar A., Sundaram R.M., Laha G.S., Qureshi I.A., Reddy G.A., Ghazi I.A. Analysis of nucleotide diversity among alleles of the major bacterial blight resistance gene Xa27 in cultivars of rice (Oryza sativa) and its wild relatives. Planta. 2013;238:293-305.

    Not in our library10.1007/s00425-013-1891-3

  82. 82.

    Chen X., Shang J., Chen D., Lei C., Zou Y., Zhai W., Liu G., Xu J., Ling Z., Cao G., et al. A B-lectin receptor kinase gene conferring rice blast resistance. Plant J. 2006;46:794-804.

    Not in our library10.1111/j.1365-313x.2006.02739.x

  83. 83.

    Collins N., Drake J., Ayliffe M., Sun Q., Ellis J., Hulbert S., Pryor T. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell. 1999;11:1365-1376.

    Not in our library10.1105/tpc.11.7.1365

  84. 84.

    Johal G.S., Briggs S.P. Reductase activity encoded by the Hm1 disease resistance gene in maize. Science. 1992;258:985-987.

    Not in our library10.1126/science.1359642

  85. 85.

    Grant M.R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R.W., Dangl J.L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995;269:843-846.

    Not in our library10.1126/science.7638602

  86. 86.

    Bent A.F., Kunkel B.N., Dahlbeck D., Brown K.L., Schmidt R., Giraudat J., Staskawicz B.J., Leung J. RPS2 of Arabidopsis thaliana: A leucine-rich repeat class of plant disease resistance genes. Science. 1994;265:1856-1860.

    Not in our library10.1126/science.8091210

  87. 87.

    McDowell J.M., Dhandaydham M., Long T.A., Aarts M.G., Goff S., Holub E.B., Dangl J.L. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell. 1998;10:1861-1874.

    Not in our library10.1105/tpc.10.11.1861

  88. 88.

    Bittner-Eddy P.D., Crute I.R., Holub E.B., Beynon J.L. RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 2000;21:177-188.

    Not in our library10.1046/j.1365-313x.2000.00664.x

  89. 89.

    Takahashi H., Miller J., Nozaki Y., Takeda M., Shah J., Hase S., Ikegami M., Ehara Y., Dinesh-Kumar S.P., Sukamto. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 2002;32:655-667.

    Not in our library10.1046/j.1365-313x.2002.01453.x

  90. 90.

    Botella M.A., Parker J.E., Frost L.N., Bittner-Eddy P.D., Beynon J.L., Daniels M.J., Holub E.B., Jones J.D. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell. 1998;10:1847-1860.

    Not in our library10.1105/tpc.10.11.1847

  91. 91.

    Van der Biezen E.A., Freddie C.T., Kahn K., Parker J.E., Jones J.D. Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. 2002;29:439-451.

    Not in our library10.1046/j.0960-7412.2001.01229.x

  92. 92.

    Gassmann W., Hinsch M.E., Staskawicz B.J. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J. 1999;20:265-277.

    Not in our library10.1046/j.1365-313x.1999.t01-1-00600.x

  93. 93.

    Noel L., Moores T.L., van Der Biezen E.A., Parniske M., Daniels M.J., Parker J.E., Jones J.D. Pronounced intraspecific haplotype divergence at the RPP5 complex disease resistance locus of Arabidopsis. Plant Cell. 1999;11:2099-2112.

    Not in our library10.1105/tpc.11.11.2099

  94. 94.

    Warren R.F., Henk A., Mowery P., Holub E., Innes R.W. A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell. 1998;10:1439-1452.

    Not in our library10.1105/tpc.10.9.1439

  95. 95.

    Deslandes L., Olivier J., Theulieres F., Hirsch J., Feng D.X., Bittner-Eddy P., Beynon J., Marco Y. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1 R gene, a member of a novel family of resistance genes. Proc. Natl. Acad. Sci. USA. 2002;99:2404-2409.

    Not in our library10.1073/pnas.032485099

  96. 96.

    Tor M., Brown D., Cooper A., Woods-Tor A., Sjolander K., Jones J.D., Holub E.B. Arabidopsis downy mildew resistance gene RPP27 encodes a receptor-like protein similar to CLAVATA2 and tomato Cf-9. Plant Physiol. 2004;135:1100-1112.

    Not in our library10.1104/pp.103.037770

  97. 97.

    Diener A.C., Ausubel F.M. Resistance to fusarium oxysporum1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics. 2005;171:305-321.

    Not in our library10.1534/genetics.105.042218

  98. 98.

    Swiderski M.R., Innes R.W. The Arabidopsis PBS1 resistance gene encodes a member of a novel protein kinase subfamily. Plant J. 2001;26:101-112.

    Not in our library10.1046/j.1365-313x.2001.01014.x

  99. 99.

    Tabata S., Kaneko T., Nakamura Y., Kotani H., Kato T., Asamizu E., Miyajima N., Sasamoto S., Kimura T., Hosouchi T., et al. Sequence and analysis of chromosome 5 of the plant Arabidopsis thaliana. Nature. 2000;408:823-826.

    Not in our library10.1038/35048507

  100. 100.

    Kim M.H., Kim Y., Kim J.W., Lee H.S., Lee W.S., Kim S.K., Wang Z.Y., Kim S.H. Identification of Arabidopsis BAK1-associating receptor-like kinase 1 (BARK1) and characterization of its gene expression and brassinosteroid-regulated root phenotypes. Plant Cell Physiol. 2013;54:1620-1634.

    Not in our library10.1093/pcp/pct106

  101. 101.

    Century K.S., Shapiro A.D., Repetti P.P., Dahlbeck D., Holub E., Staskawicz B.J. NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science. 1997;278:1963-1965.

    Not in our library10.1126/science.278.5345.1963

  102. 102.

    Xiao S., Ellwood S., Calis O., Patrick E., Li T., Coleman M., Turner J.G. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science. 2001;291:118-120.

    Not in our library10.1126/science.291.5501.118

  103. 103.

    Lawrence G.J., Finnegan E.J., Ayliffe M.A., Ellis J.G. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell. 1995;7:1195-1206.

    Not in our library10.1105/tpc.7.8.1195

  104. 104.

    Ellis J.G., Lawrence G.J., Luck J.E., Dodds P.N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell. 1999;11:495-506.

    Not in our library10.1105/tpc.11.3.495

  105. 105.

    Anderson P.A., Lawrence G.J., Morrish B.C., Ayliffe M.A., Finnegan E.J., Ellis J.G. Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. Plant Cell. 1997;9:641-651.

    Not in our library10.1105/tpc.9.4.641

  106. 106.

    Dodds P.N., Lawrence G.J., Ellis J.G. Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell. 2001;13:163-178.

    Not in our library10.1105/tpc.13.1.163

  107. 107.

    Cai D., Kleine M., Kifle S., Harloff H.J., Sandal N.N., Marcker K.A., Klein-Lankhorst R.M., Salentijn E.M., Lange W., Stiekema W.J., et al. Positional cloning of a gene for nematode resistance in sugar beet. Science. 1997;275:832-834.

    Not in our library10.1126/science.275.5301.832

  108. 108.

    Whitham S., Dinesh-Kumar S.P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell. 1994;78:1101-1115.

    Not in our library10.1016/0092-8674(94)90283-6

  109. 109.

    Meyers B.C. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell. 2003;15:809-834.

    Not in our library10.1105/tpc.009308

  110. 110.

    Fritz-Laylin L.K., Krishnamurthy N., Tor M., Sjolander K.V., Jones J.D. Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiol. 2005;138:611-623.

    Not in our library10.1104/pp.104.054452

  111. 111.

    Yu J., Tehrim S., Zhang F., Tong C., Huang J., Cheng X., Dong C., Zhou Y., Qin R., Hua W., et al. Genome-wide comparative analysis of NBS-encoding genes between Brassica species and Arabidopsis thaliana. BMC Genom. 2014;15:3-21.

    Not in our library10.1186/1471-2164-15-3

  112. 112.

    Shiu S.H., Karlowski W.M., Pan R., Tzeng Y.H., Mayer K.F., Li W.H. Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell. 2004;16:1220-1234.

    Not in our library10.1105/tpc.020834

  113. 113.

    Lurin C., Andres C., Aubourg S., Bellaoui M., Bitton F., Bruyere C., Caboche M., Debast C., Gualberto J., Hoffmann B., et al. Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell. 2004;16:2089-2103.

    Not in our library10.1105/tpc.104.022236

  114. 114.

    Guo Y.L., Fitz J., Schneeberger K., Ossowski S., Cao J., Weigel D. Genome-wide comparison of nucleotide-binding site-leucine-rich repeat-encoding genes in Arabidopsis. Plant Physiol. 2011;157:757-769.

    Not in our library10.1104/pp.111.181990

  115. 115.

    Kohler A., Rinaldi C., Duplessis S., Baucher M., Geelen D., Duchaussoy F., Meyers B.C., Boerjan W., Martin F. Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol. Biol. 2008;66:619-636.

    Not in our library10.1007/s11103-008-9293-9

  116. 116.

    Zan Y., Ji Y., Zhang Y., Yang S., Song Y., Wang J. Genome-wide identification, characterization and expression analysis of populus leucine-rich repeat receptor-like protein kinase genes. BMC Genom. 2013;14:318-331.

    Not in our library10.1186/1471-2164-14-318

  117. 117.

    Tuskan G.A., Difazio S., Jansson S., Bohlmann J., Grigoriev I., Hellsten U., Putnam N., Ralph S., Rombauts S., Salamov A., et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006;313:1596-1604.

    Not in our library10.1126/science.1128691

  118. 118.

    Yang S., Zhang X., Yue J.X., Tian D., Chen J.Q. Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol. Genet. Genom. 2008;280:187-198.

    Not in our library10.1007/s00438-008-0355-0

  119. 119.

    Kale S.M., Pardeshi V.C., Barvkar V.T., Gupta V.S., Kadoo N.Y. Genome-wide identification and characterization of nucleotide binding site leucine-rich repeat genes in linseed reveal distinct patterns of gene structure. Genome. 2013;56:91-99.

    Not in our library10.1139/gen-2012-0135

  120. 120.

    Andolfo G., Sanseverino W., Aversano R., Frusciante L., Ercolano M.R. Genome-wide identification and analysis of candidate genes for disease resistance in tomato. Mol. Breed. 2013;33:227-233.

    Not in our library10.1007/s11032-013-9928-7

  121. 121.

    Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature. 2012;485:635-641.

    Not in our library10.1038/nature11119

  122. 122.

    Ming R., Hou S., Feng Y., Yu Q., Dionne-Laporte A., Saw J.H., Senin P., Wang W., Ly B.V., Lewis K.L., et al. The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature. 2008;452:991-996.

    Not in our library10.1038/nature06856

  123. 123.

    Yang L., Li D., Li Y., Gu X., Huang S., Garcia-Mas J., Weng Y. A 1,681-locus consensus genetic map of cultivated cucumber including 67 NB-LRR resistance gene homolog and ten gene loci. BMC Plant Biol. 2013;13:53.

    Not in our library10.1186/1471-2229-13-53

  124. 124.

    Lozano R., Ponce O., Ramirez M., Mostajo N., Orjeda G. Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS ONE. 2012;7:e34775.

    Not in our library10.1371/journal.pone.0034775

  125. 125.

    Wei H., Li W., Sun X., Zhu S., Zhu J. Systematic analysis and comparison of nucleotide-binding site disease resistance genes in a diploid cotton Gossypium raimondii. PLoS ONE. 2013;8:e68435.

    Not in our library10.1371/journal.pone.0068435

  126. 126.

    Chen J.Y., Huang J.Q., Li N.Y., Ma X.F., Wang J.L., Liu C., Liu Y.F., Liang Y., Bao Y.M., Dai X.F. Genome-wide analysis of the gene families of resistance gene analogues in cotton and their response to Verticillium wilt. BMC Plant Biol. 2015;15:148.

    Not in our library10.1186/s12870-015-0508-3

  127. 127.

    Li J., Zhang Q.Y., Gao Z.H., Wang F., Duan K., Ye Z.W., Gao Q.H. Genome-wide identification and comparative expression analysis of NBS-LRR-encoding genes upon Colletotrichum gloeosporioides infection in two ecotypes of Fragaria vesca. Gene. 2013;527:215-227.

    Not in our library10.1016/j.gene.2013.06.008

  128. 128.

    Li X., Cheng Y., Ma W., Zhao Y., Jiang H., Zhang M. Identification and characterization of NBS-encoding disease resistance genes in Lotus japonicus. Plant Syst. Evol. 2010;289:101-110.

    Not in our library10.1007/s00606-010-0331-0

  129. 129.

    Xue J.Y., Wang Y., Wu P., Wang Q., Yang L.T., Pan X.H., Wang B., Chen J.Q. A primary survey on bryophyte species reveals two novel classes of nucleotide-binding site (NBS) genes. PLoS ONE. 2012;7:e36700.

    Not in our library10.1371/journal.pone.0036700

  130. 130.

    O’Toole N., Hattori M., Andres C., Iida K., Lurin C., Schmitz-Linneweber C., Sugita M., Small I. On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 2008;25:1120-1128.

    Not in our library10.1093/molbev/msn057

  131. 131.

    Zhou T., Wang Y., Chen J.Q., Araki H., Jing Z., Jiang K., Shen J., Tian D. Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol. Genet. Genom. 2004;271:402-415.

    Not in our library10.1007/s00438-004-0990-z

  132. 132.

    Dardick C., Chen J., Richter T., Ouyang S., Ronald P. The rice kinase database. A phylogenomic database for the rice kinome. Plant Physiol. 2007;143:579-586.

    Not in our library10.1104/pp.106.087270

  133. 133.

    Singh S., Chand S., Singh N.K., Sharma T.R. Genome-wide distribution, organisation and functional characterization of disease resistance and defence response genes across rice species. PLoS ONE. 2015;10:e0125964.

    Not in our library10.1371/journal.pone.0125964

  134. 134.

    Bouktila D., Khalfallah Y., Habachi-Houimli Y., Mezghani-Khemakhem M., Makni M., Makni H. Large-scale analysis of NBS domain-encoding resistance gene analogs in Triticeae. Genet. Mol. Biol. 2014;37:598-610.

    Not in our library10.1590/s1415-47572014000400017

  135. 135.
    Transcript profiles of maize embryo sacs and preliminary identification of genes involved in the embryo sac–pollen tube interaction · 2014
    Not checked
  136. 136.

    Cheng Y., Li X., Jiang H., Ma W., Miao W., Yamada T., Zhang M. Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize. FEBS J. 2012;279:2431-2443.

    Not in our library10.1111/j.1742-4658.2012.08621.x

  137. 137.

    Mace E., Tai S., Innes D., Godwin I., Hu W., Campbell B., Gilding E., Cruickshank A., Prentis P., Wang J., et al. The plasticity of NBS resistance genes in sorghum is driven by multiple evolutionary processes. BMC Plant Biol. 2014;14:253-266.

    Not in our library10.1186/s12870-014-0253-z

  138. 138.

    Cheng X., Jiang H., Zhao Y., Qian Y., Zhu S., Cheng B. A genomic analysis of disease-resistance genes encoding nucleotide binding sites in Sorghum bicolor. Genet. Mol. Biol. 2010;33:292-297.

    Not in our library10.1590/s1415-47572010005000036

  139. 139.

    International Barley Genome Sequencing Consortium. A physical, genetic and functional sequence assembly of the barley genome. Nature. 2012;491:711-716.

    Not in our library10.1038/nature11543

  140. 140.

    Gu L., Si W., Zhao L., Yang S., Zhang X. Dynamic evolution of NBS-LRR genes in bread wheat and its progenitors. Mol. Genet. Genom. 2015;290:727-738.

    Not in our library10.1007/s00438-014-0948-8

  141. 141.

    Tan S., Wu S. Genome wide analysis of nucleotide-binding site disease resistance genes in Brachypodium distachyon. Comp. Funct. Genom. 2012;2012:418208-418220.

    Not in our library10.1155/2012/418208

  142. 142.

    Ling H.Q., Zhao S., Liu D., Wang J., Sun H., Zhang C., Fan H., Li D., Dong L., Tao Y., et al. Draft genome of the wheat A-genome progenitor Triticum urartu. Nature. 2013;496:87-90.

    Not in our library10.1038/nature11997

  143. 143.

    Jia J., Zhao S., Kong X., Zhao G., He W., Appels R., Pfeifer M., Tao Y., Zhang X., Li Y., et al. Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature. 2013;496:91-95.

    Not in our library10.1038/nature12028

  144. 144.

    Michael T.P., Jackson S. The first 50 plant genomes. Plant Gen. 2013;6.

    Not in our library10.3835/plantgenome2013.03.0001in

  145. 145.

    Hammond-Kosack K.E., Jones J.D. Plant disease resistance genes. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1997;48:575-607.

    Not in our library10.1146/annurev.arplant.48.1.575

  146. 146.

    Chisholm S.T., Coaker G., Day B., Staskawicz B.J. Host-microbe interactions: Shaping the evolution of the plant immune response. Cell. 2006;124:803-814.

    Not in our library10.1016/j.cell.2006.02.008

  147. 147.

    Maekawa T., Cheng W., Spiridon L.N., Toller A., Lukasik E., Saijo Y., Liu P., Shen Q.H., Micluta M.A., Somssich I.E., et al. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe. 2011;9:187-199.

    Not in our library10.1016/j.chom.2011.02.008

  148. 148.

    Alber T. Structure of the leucine zipper. Curr. Opin. Genet. Dev. 1992;2:205-210.

    Not in our library10.1016/s0959-437x(05)80275-8

  149. 149.

    Bent A.F. Plant disease resistance genes: Function meets structure. Plant Cell. 1996;8:1757-1771.

    Not in our library10.1105/tpc.8.10.1757

  150. 150.

    Martin G.B., Bogdanove A.J., Sessa G. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 2003;54:23-61.

    Not in our library10.1146/annurev.arplant.54.031902.135035

  151. 151.

    Tameling W.I., Elzinga S.D., Darmin P.S., Vossen J.H., Takken F.L., Haring M.A., Cornelissen B.J. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell. 2002;14:2929-2939.

    Not in our library10.1105/tpc.005793

  152. 152.

    Van Ooijen G., van den Burg H.A., Cornelissen B.J., Takken F.L. Structure and function of resistance proteins in solanaceous plants. Annu. Rev. Phytopathol. 2007;45:43-72.

    Not in our library10.1146/annurev.phyto.45.062806.094430

  153. 153.

    Rairdan G.J., Collier S.M., Sacco M.A., Baldwin T.T., Boettrich T., Moffett P. The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell. 2008;20:739-751.

    Not in our library10.1105/tpc.107.056036

  154. 154.

    Collier S.M., Hamel L.P., Moffett P. Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol. Plant Microbe Interact. 2011;24:918-931.

    Not in our library10.1094/mpmi-03-11-0050

  155. 155.

    Meyers B.C., Dickerman A.W., Michelmore R.W., Sivaramakrishnan S., Sobral B.W., Young N.D. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 1999;20:317-332.

    Not in our library10.1046/j.1365-313x.1999.t01-1-00606.x

  156. 156.

    Meyers B.C., Morgante M., Michelmore R.W. TIR-X and TIR-NBS proteins: Two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J. 2002;32:77-92.

    Not in our library10.1046/j.1365-313x.2002.01404.x

  157. 157.

    Leipe D.D., Koonin E.V., Aravind L. STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: Multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J. Mol. Biol. 2004;343:1-28.

    Not in our library10.1016/j.jmb.2004.08.023

  158. 158.

    Pan Q., Wendel J., Fluhr R. Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J. Mol. Evol. 2000;50:203-213.

    Not in our library10.1007/s002399910023

  159. 159.

    Takken F.L., Albrecht M., Tameling W.I. Resistance proteins: Molecular switches of plant defence. Curr. Opin. Plant Biol. 2006;9:383-390.

    Not in our library10.1016/j.pbi.2006.05.009

  160. 160.

    Lukasik E., Takken F.L. STANDing strong, resistance proteins instigators of plant defence. Curr. Opin. Plant Biol. 2009;12:427-436.

    Not in our library10.1016/j.pbi.2009.03.001

  161. 161.

    Takken F.L., Goverse A. How to build a pathogen detector: Structural basis of NB-LRR function. Curr. Opin. Plant Biol. 2012;15:375-384.

    Not in our library10.1016/j.pbi.2012.05.001

  162. 162.

    Deslandes L., Rivas S. Catch me if you can: Bacterial effectors and plant targets. Trends Plant Sci. 2012;17:644-655.

    Not in our library10.1016/j.tplants.2012.06.011

  163. 163.

    Heidrich K., Wirthmueller L., Tasset C., Pouzet C., Deslandes L., Parker J.E. Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science. 2011;334:1401-1404.

    Not in our library10.1126/science.1211641

  164. 164.

    Bhattacharjee S., Halane M.K., Kim S.H., Gassmann W. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science. 2011;334:1405-1408.

    Not in our library10.1126/science.1211592

  165. 165.

    Zhang Z., Wu Y., Gao M., Zhang J., Kong Q., Liu Y., Ba H., Zhou J., Zhang Y. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe. 2012;11:253-263.

    Not in our library10.1016/j.chom.2012.01.015

  166. 166.

    Meng X., Zhang S. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 2013;51:245-266.

    Not in our library10.1146/annurev-phyto-082712-102314

  167. 167.

    Buscaill P., Rivas S. Transcriptional control of plant defence responses. Curr. Opin. Plant Biol. 2014;20:35-46.

    Not in our library10.1016/j.pbi.2014.04.004

  168. 168.

    Cui H., Tsuda K., Parker J.E. Effector-triggered immunity: From pathogen perception to robust defense. Annu. Rev. Plant Biol. 2015;66:487-511.

    Not in our library10.1146/annurev-arplant-050213-040012

  169. 169.

    Williams S.J., Sohn K.H., Wan L., Bernoux M., Sarris P.F., Segonzac C., Ve T., Ma Y., Saucet S.B., Ericsson D.J., et al. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science. 2014;344:299-303.

    Not in our library10.1126/science.1247357

  170. 170.

    Chinchilla D., Zipfel C., Robatzek S., Kemmerling B., Nurnberger T., Jones J.D., Felix G., Boller T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature. 2007;448:497-500.

    Not in our library10.1038/nature05999

  171. 171.

    Stergiopoulos I., de Wit P.J. Fungal effector proteins. Annu. Rev. Phytopathol. 2009;47:233-263.

    Not in our library10.1146/annurev.phyto.112408.132637

  172. 172.

    Panstruga R., Dodds P.N. Terrific protein traffic: The mystery of effector protein delivery by filamentous plant pathogens. Science. 2009;324:748-750.

    Not in our library10.1126/science.1171652

  173. 173.

    Wang W., Zhang Y., Wen Y., Berkey R., Ma X., Pan Z., Bendigeri D., King H., Zhang Q., Xiao S. A comprehensive mutational analysis of the Arabidopsis resistance protein RPW8.2 reveals key amino acids for defense activation and protein targeting. Plant Cell. 2013;25:4242-4261.

    Not in our library10.1105/tpc.113.117226

  174. 174.

    Zhai J., Jeong D.H., de Paoli E., Park S., Rosen B.D., Li Y., Gonzalez A.J., Yan Z., Kitto S.L., Grusak M.A., et al. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 2011;25:2540-2553.

    Not in our library10.1101/gad.177527.111

  175. 175.

    Zhao M., Cai C., Zhai J., Lin F., Li L., Shreve J., Thimmapuram J., Hughes T.J., Meyers B.C., Ma J. Coordination of microRNAs, phasiRNAs, and NB-LRR genes in response to a plant pathogen: Insights from analyses of a set of soybean Rps gene near isogenic lines. Plant Gen. 2015;8.

    Not in our library10.3835/plantgenome2014.09.0044

  176. 176.

    Shivaprasad P.V., Chen H.M., Patel K., Bond D.M., Santos B.A., Baulcombe D.C. A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell. 2012;24:859-874.

    Not in our library10.1105/tpc.111.095380

  177. 177.

    Liu W., Liu J., Triplett L., Leach J.E., Wang G.L. Novel insights into rice innate immunity against bacterial and fungal pathogens. Annu. Rev. Phytopathol. 2014;52:213-241.

    Not in our library10.1146/annurev-phyto-102313-045926

  178. 178.

    Afzal A.J., Wood A.J., Lightfoot D.A. Plant receptor-like serine threonine kinases: Roles in signaling and plant defense. Mol. Plant Microbe Interact. 2008;21:507-517.

    Not in our library10.1094/mpmi-21-5-0507

  179. 179.

    Bleecker A.B., Kende H. Ethylene: A gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 2000;16:1-18.

    Not in our library10.1146/annurev.cellbio.16.1.1

  180. 180.

    Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., Tabata S., Shinozaki K., Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 2001;409:1060-1063.

    Not in our library10.1038/35059117

  181. 181.

    Becraft P.W. Receptor kinase signaling in plant development. Annu. Rev. Cell Dev. Biol. 2002;18:163-192.

    Not in our library10.1146/annurev.cellbio.18.012502.083431

  182. 182.

    Lee S.W., Han S.W., Sririyanum M., Park C.J., Seo Y.S., Ronald P.C. A type I-secreted, sulfated peptide triggers Xa21-mediated innate immunity. Science. 2009;326:850-853.

    Not in our library10.1126/science.1173438

  183. 183.

    Hu H., Wang J., Shi C., Yuan C., Peng C., Yin J., Li W., He M., Wang J., Ma B. A receptor like kinase gene with expressional responsiveness on Xanthomonas oryzae pv. oryzae is essential for Xa21-mediated disease resistance. Rice. 2015;8:1-9.

    Not in our library10.1186/s12284-014-0034-1

  184. 184.

    Peng Y., Bartley L.E., Chen X., Dardick C., Chern M., Ruan R., Canlas P.E., Ronald P.C. OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol. Plant. 2008;1:446-458.

    Not in our library10.1093/mp/ssn024

  185. 185.

    Nekrasov V., Ludwig A.A., Jones J.D. CITRX thioredoxin is a putative adaptor protein connecting Cf-9 and the ACIK1 protein kinase during the Cf-9/Avr9 induced defence response. FEBS Lett. 2006;580:4236-4241.

    Not in our library10.1016/j.febslet.2006.06.077

  186. 186.

    Rivas S., Rougon-Cardoso A., Smoker M., Schauser L., Yoshioka H., Jones J.D. CITRX thioredoxin interacts with the tomato Cf-9 resistance protein and negatively regulates defence. EMBO J. 2004;23:2156-2165.

    Not in our library10.1038/sj.emboj.7600224

  187. 187.

    Gabriels S.H., Ekengren S.K., van Ooijen G., Abd-El-Haliem A.M., van den Berg G.C., Vossen J.H., Rainey D.Y., Martin G.B., Takken F.L., de Wit P.J., et al. An NB-LRR protein required for HR signalling mediated by both extra and intracellular resistance proteins. Plant J. 2007;50:14-28.

    Not in our library10.1111/j.1365-313x.2007.03027.x

  188. 188.

    Radutoiu S., Madsen L.H., Madsen E.B., Felle H.H., Umehara Y., Gronlund M., Sato S., Nakamura Y., Tabata S., Sandal N., et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature. 2003;425:585-592.

    Not in our library10.1038/nature02039

  189. 189.

    Madsen E.B., Madsen L.H., Radutoiu S., Olbryt M., Rakwalska M., Szczyglowski K., Sato S., Kaneko T., Tabata S., Sandal N., et al. A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature. 2003;425:637-640.

    Not in our library10.1038/nature02045

  190. 190.

    Jeong S., Trotochaud A.E., Clark S.E. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Plant Cell. 1999;11:1925-1934.

    Not in our library10.1105/tpc.11.10.1925

  191. 191.

    Nadeau J.A., Sack F.D. Control of stomatal distribution on the Arabidopsis leaf surface. Science. 2002;296:1697-1700.

    Not in our library10.1126/science.1069596

  192. 192.

    Ogawa M., Shinohara H., Sakagami Y., Matsubayashi Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science. 2008;319:294.

    Not in our library10.1126/science.1150083

  193. 193.

    Rojo E., Sharma V.K., Kovaleva V., Raikhel N.V., Fletcher J.C. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. Plant Cell. 2002;14:969-977.

    Not in our library10.1105/tpc.002196

  194. 194.

    Trotochaud A.E., Hao T., Wu G., Yang Z., Clark S.E. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell. 1999;11:393-406.

    Not in our library10.1105/tpc.11.3.393

  195. 195.

    Lee J.S., Kuroha T., Hnilova M., Khatayevich D., Kanaoka M.M., McAbee J.M., Sarikaya M., Tamerler C., Torii K.U. Direct interaction of ligand-receptor pairs specifying stomatal patterning. Genes Dev. 2012;26:126-136.

    Not in our library10.1101/gad.179895.111

  196. 196.

    Bai J., Pennill L.A., Ning J., Lee S.W., Ramalingam J., Webb C.A., Zhao B., Nelson J.C., Sun Q., Leach J.E., et al. Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res. 2002;12:1871-1884.

    Not in our library10.1101/gr.454902

  197. 197.
    <it>In silico</it> approach to predict candidate R proteins and to define their domain architecture · 2012
    Not checked
  198. 198.

    Gururani M.A., Venkatesh J., Upadhyaya C.P., Nookaraju A., Pandey S.K., Park S.W. Plant disease resistance genes: Current status and future directions. Physiol. Mol. Plant Pathol. 2012;78:51-65.

    Not in our library10.1016/j.pmpp.2012.01.002

  199. 199.

    Xiao S., Emerson B., Ratanasut K., Patrick E., O’Neill C., Bancroft I., Turner J.G. Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Mol. Biol. Evol. 2004;21:1661-1672.

    Not in our library10.1093/molbev/msh165

  200. 200.

    Ma X.F., Li Y., Sun J.L., Wang T.T., Fan J., Lei Y., Huang Y.Y., Xu Y.J., Zhao J.Q., Xiao S., et al. Ectopic expression of resistance to powdery mildew8.1 confers resistance to fungal and oomycete pathogens in Arabidopsis. Plant Cell Physiol. 2014;55:1484-1496.

    Not in our library10.1093/pcp/pcu080

  201. 201.

    Panstruga R. Discovery of novel conserved peptide domains by ortholog comparison within plant multi-protein families. Plant Mol. Biol. 2005;59:485-500.

    Not in our library10.1007/s11103-005-0353-0

  202. 202.

    Wretblad S., Bohman S., Dixelius C. Overexpression of a Brassica nigra cDNA gives enhanced resistance to Leptosphaeria maculans in B. napus. Mol. Plant Microbe Interact. 2003;16:477-484.

    Not in our library10.1094/mpmi.2003.16.6.477

  203. 203.

    Brandwagt B.F., Kneppers T.J., Nijkamp H.J., Hille J. Overexpression of the tomato Asc-1 gene mediates high insensitivity to AAL toxins and fumonisin B1 in tomato hairy roots and confers resistance to Alternaria alternata f. sp. lycopersici in Nicotiana umbratica plants. Mol. Plant Microbe Interact. 2002;15:35-42.

    Not in our library10.1094/mpmi.2002.15.1.35

  204. 204.

    Spassieva S.D., Markham J.E., Hille J. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AAL-toxin-induced programmed cell death. Plant J. 2002;32:561-572.

    Not in our library10.1046/j.1365-313x.2002.01444.x

  205. 205.

    Scofield S.R., Tobias C.M., Rathjen J.P., Chang J.H., Lavelle D.T., Michelmore R.W., Staskawicz B.J. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science. 1996;274:2063-2065.

    Not in our library10.1126/science.274.5295.2063

  206. 206.

    Tang X., Frederick R.D., Zhou J., Halterman D.A., Jia Y., Martin G.B. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science. 1996;274:2060-2063.

    Not in our library10.1126/science.274.5295.2060

  207. 207.

    Nomura H., Komori T., Uemura S., Kanda Y., Shimotani K., Nakai K., Furuichi T., Takebayashi K., Sugimoto T., Sano S., et al. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. Nat. Commun. 2012;3:926-925.

    Not in our library10.1038/ncomms1926

  208. 208.

    Amirsadeghi S., Robson C.A., Vanlerberghe G.C. The role of the mitochondrion in plant responses to biotic stress. Physiol. Plant. 2007;129:253-266.

    Not in our library10.1111/j.1399-3054.2006.00775.x

  209. 209.

    Dahan J., Mireau H. The Rf and Rf-like PPR in higher plants, a fast-evolving subclass of PPR genes. RNA Biol. 2013;10:1469-1476.

    Not in our library10.4161/rna.25568

  210. 210.

    Schmitz-Linneweber C., Small I. Pentatricopeptide repeat proteins: A socket set for organelle gene expression. Trends Plant Sci. 2008;13:663-670.

    Not in our library10.1016/j.tplants.2008.10.001

  211. 211.

    Jonietz C., Forner J., Holzle A., Thuss S., Binder S. RNA processing factors2 is required for 5′ end processing of nad9 and cox3 mRNAs in mitochondria of Arabidopsis thaliana. Plant Cell. 2010;22:443-453.

    Not in our library10.1105/tpc.109.066944

  212. 212.

    Jonietz C., Forner J., Hildebrandt T., Binder S. RNA processing factor3 is crucial for the accumulation of mature ccmC transcripts in mitochondria of Arabidopsis accession columbia. Plant Physiol. 2011;157:1430-1439.

    Not in our library10.1104/pp.111.181552

  213. 213.

    Cui X., Wise R.P., Schnable P.S. The rf2 nuclear restorer gene of male-sterile T-cytoplasm maize. Science. 1996;272:1334-1336.

    Not in our library10.1126/science.272.5266.1334

  214. 214.

    Wang Z., Zou Y., Li X., Zhang Q., Chen L., Wu H., Su D., Chen Y., Guo J., Luo D., et al. Cytoplasmic male sterility of rice with boro II cytoplasm is caused by a cytotoxic peptide and is restored by two related PPR motif genes via distinct modes of mRNA silencing. Plant Cell. 2006;18:676-687.

    Not in our library10.1105/tpc.105.038240

  215. 215.

    Park Y.J., Lee H.J., Kwak K.J., Lee K., Hong S.W., Kang H. MicroRNA400-guided cleavage of pentatricopeptide repeat protein mRNAs renders Arabidopsis thaliana more susceptible to pathogenic bacteria and fungi. Plant Cell Physiol. 2014;55:1660-1668.

    Not in our library10.1093/pcp/pcu096

  216. 216.
    Mediated plastid RNA editing in plant immunity. · 2013
    Not checked
  217. 217.

    Shirasu K., Lahaye T., Tan M.W., Zhou F., Azevedo C., Schulze-Lefert P. A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell. 1999;99:355-366.

    Not in our library10.1016/s0092-8674(00)81522-6

  218. 218.
    A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1 · 2000
    Not checked
  219. 219.

    Liu B., Li J.F., Ao Y., Qu J., Li Z., Su J., Zhang Y., Liu J., Feng D., Qi K., et al. Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell. 2012;24:3406-3419.

    Not in our library10.1105/tpc.112.102475

  220. 220.

    Chisholm S.T., Mahajan S.K., Whitham S.A., Yamamoto M.L., Carrington J.C. Cloning of the Arabidopsis RTM1 gene, which controls restriction of long-distance movement of tobacco etch virus. Proc. Natl. Acad. Sci. USA. 2000;97:489-494.

    Not in our library10.1073/pnas.97.1.489

  221. 221.

    Ouibrahim L., Mazier M., Estevan J., Pagny G., Decroocq V., Desbiez C., Moretti A., Gallois J.L., Caranta C. Cloning of the Arabidopsis rwm1 gene for resistance to watermelon mosaic virus points to a new function for natural virus resistance genes. Plant J. 2014;79:705-716.

    Not in our library10.1111/tpj.12586

  222. 222.
    EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases · 1999
    Not checked
  223. 223.

    Cao H., Glazebrook J., Clarke J.D., Volko S., Dong X. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997;88:57-63.

    Not in our library10.1016/s0092-8674(00)81858-9

  224. 224.

    Dickman M.B., Fluhr R. Centrality of host cell death in plant-microbe interactions. Annu. Rev. Phytopathol. 2013;51:543-570.

    Not in our library10.1146/annurev-phyto-081211-173027

  225. 225.

    O’Brien J.A., Daudi A., Finch P., Butt V.S., Whitelegge J.P., Souda P., Ausubel F.M., Bolwell G.P. A peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense. Plant Physiol. 2012;158:2013-2027.

    Not in our library10.1104/pp.111.190140

  226. 226.

    Daudi A., Cheng Z., O’Brien J.A., Mammarella N., Khan S., Ausubel F.M., Bolwell G.P. The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity. Plant Cell. 2012;24:275-287.

    Not in our library10.1105/tpc.111.093039

  227. 227.

    Bindschedler L.V., Dewdney J., Blee K.A., Stone J.M., Asai T., Plotnikov J., Denoux C., Hayes T., Gerrish C., Davies D.R., et al. Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J. 2006;47:851-863.

    Not in our library10.1111/j.1365-313x.2006.02837.x

  228. 228.

    Mohanta T.K., Arora P.K., Mohanta N., Parida P., Bae H. Identification of new members of the MAPK gene family in plants shows diverse conserved domains and novel activation loop variants. BMC Genom. 2015;16:58-77.

    Not in our library10.1186/s12864-015-1244-7

  229. 229.

    Bolser D.M., Kerhornou A., Walts B., Kersey P. Triticeae resources in Ensembl Plants. Plant Cell Physiol. 2015;56:e3.

    Not in our library10.1093/pcp/pcu183

  230. 230.

    Peng W., Wang J., Cai J., Chen L., Li M., Wu F.X. Improving protein function prediction using domain and protein complexes in PPI networks. BMC Syst. Biol. 2014;8:35-47.

    Not in our library10.1186/1752-0509-8-35

  231. 231.

    Bailey T.L., Williams N., Misleh C., Li W.W. MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34:W369-W373.

    Not in our library10.1093/nar/gkl198

  232. 232.
    Hidden Markov Models and their Applications in Biological Sequence Analysis · 2009
    No notice
  233. 233.

    Schultz J., Copley R.R., Doerks T., Ponting C.P., Bork P. SMART: A web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 2000;28:231-234.

    Not in our library10.1093/nar/28.1.231

  234. 234.

    Pruitt K.D., Tatusova T., Klimke W., Maglott D.R. NCBI reference sequences: Current status, policy and new initiatives. Nucleic Acids Res. 2009;37:D32-D36.

    Not in our library10.1093/nar/gkn721

  235. 235.

    Sanseverino W., Roma G., de Simone M., Faino L., Melito S., Stupka E., Frusciante L., Ercolano M.R. PRGdb: A bioinformatics platform for plant resistance gene analysis. Nucleic Acids Res. 2010;38:D814-D821.

    Not in our library10.1093/nar/gkp978

  236. 236.
    Accelerated Profile HMM Searches · 2011
    No notice
  237. 237.

    Bailey T.L., Elkan C. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1994;2:28-36.

    Not in our library

  238. 238.

    Liu Y., Schmidt B., Liu W., Maskell D.L. CUDA-MEME: Accelerating motif discovery in biological sequences using CUDA-enabled graphics processing units. Pattern Recogn. Lett. 2010;31:2170-2177.

    Not in our library10.1016/j.patrec.2009.10.009

  239. 239.
    BLAST+: architecture and applications · 2009
    No notice
  240. 240.

    Zdobnov E.M., Apweiler R. InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics. 2001;17:847-848.

    Not in our library10.1093/bioinformatics/17.9.847

  241. 241.

    Kall L., Krogh A., Sonnhammer E.L. A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 2004;338:1027-1036.

    Not in our library10.1016/j.jmb.2004.03.016

  242. 242.

    Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 2001;305:567-580.

    Not in our library10.1006/jmbi.2000.4315

  243. 243.

    Lupas A., van Dyke M., Stock J. Predicting coiled coils from protein sequences. Science. 1991;252:1162-1164.

    Not in our library10.1126/science.252.5009.1162

  244. 244.

    Radwan O., Gandhi S., Heesacker A., Whitaker B., Taylor C., Plocik A., Kesseli R., Kozik A., Michelmore R.W., Knapp S.J. Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol. Genet. Genom. 2008;280:111-125.

    Not in our library10.1007/s00438-008-0346-1

  245. 245.

    Porter B.W., Paidi M., Ming R., Alam M., Nishijima W.T., Zhu Y.J. Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol. Genet. Genom. 2009;281:609-626.

    Not in our library10.1007/s00438-009-0434-x

  246. 246.

    McDowell J.M., Simon S.A. Recent insights into R gene evolution. Mol. Plant Pathol. 2006;7:437-448.

    Not in our library10.1111/j.1364-3703.2006.00342.x

  247. 247.

    Tarr D.E., Alexander H.M. TIR-NBS-LRR genes are rare in monocots: Evidence from diverse monocot orders. BMC Res. Notes. 2009;2:197-206.

    Not in our library10.1186/1756-0500-2-197

  248. 248.

    Kim J., Lim C.J., Lee B.W., Choi J.P., Oh S.K., Ahmad R., Kwon S.Y., Ahn J., Hur C.G. A genome-wide comparison of NB-LRR type of resistance gene analogs (RGA) in the plant kingdom. Mol. Cells. 2012;33:385-392.

    Not in our library10.1007/s10059-012-0003-8

  249. 249.

    Glazebrook J. Genes controlling expression of defense responses in Arabidopsis—2001 status. Curr. Opin. Plant Biol. 2001;4:301-308.

    Not in our library10.1016/s1369-5266(00)00177-1

  250. 250.

    Yue J.X., Meyers B.C., Chen J.Q., Tian D., Yang S. Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol. 2012;193:1049-1063.

    Not in our library10.1111/j.1469-8137.2011.04006.x

  251. 251.

    Chelkowski J., Koczyk G. Resistance gene analogues of Arabidopsis thaliana: Recognition by structure. J. Appl. Genet. 2003;44:311-321.

    Not in our library

  252. 252.

    Luo S., Zhang Y., Hu Q., Chen J., Li K., Lu C., Liu H., Wang W., Kuang H. Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol. 2012;159:197-210.

    Not in our library10.1104/pp.111.192062

  253. 253.

    Pan Q., Liu Y.S., Budai-Hadrian O., Sela M., Carmel-Goren L., Zamir D., Fluhr R. Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: Tomato and arabidopsis. Genetics. 2000;155:309-322.

    Not in our library10.1093/genetics/155.1.309

  254. 254.

    Liu J.J., Ekramoddoullah A.K. Isolation, genetic variation and expression of TIR-NBS-LRR resistance gene analogs from western white pine (Pinus monticola Dougl. ex. D. Don.). Mol. Genet. Genom. 2003;270:432-441.

    Not in our library10.1007/s00438-003-0940-1

  255. 255.
    Plant Nucleotide Binding Site–Leucine-Rich Repeat (NBS-LRR) Genes: Active Guardians in Host Defense Responses · 2013
    No notice
  256. 256.

    Monosi B., Wisser R.J., Pennill L., Hulbert S.H. Full-genome analysis of resistance gene homologues in rice. Theor. Appl. Genet. 2004;109:1434-1447.

    Not in our library10.1007/s00122-004-1758-x

  257. 257.

    Michelmore R.W., Meyers B.C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998;8:1113-1130.

    Not in our library10.1101/gr.8.11.1113

  258. 258.

    Hall B.G. Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol. 2013;30:1229-1235.

    Not in our library10.1093/molbev/mst012

  259. 259.

    Young N.D. The genetic architecture of resistance. Curr. Opin. Plant Biol. 2000;3:285-290.

    Not in our library10.1016/s1369-5266(00)00081-9

  260. 260.

    Zhou B., Dolan M., Sakai H., Wang G.L. The genomic dynamics and evolutionary mechanism of the Pi2/9 locus in rice. Mol. Plant Microbe Interact. 2007;20:63-71.

    Not in our library10.1094/mpmi-20-0063

  261. 261.

    Yang S., Feng Z., Zhang X., Jiang K., Jin X., Hang Y., Chen J.Q., Tian D. Genome-wide investigation on the genetic variations of rice disease resistance genes. Plant Mol. Biol. 2006;62:181-193.

    Not in our library10.1007/s11103-006-9012-3

  262. 262.
    Identification and localisation of the NB-LRR gene family within the potato genome · 2012
    No notice
  263. 263.

    Wei F., Wing R.A., Wise R.P. Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell. 2002;14:1903-1917.

    Not in our library10.1105/tpc.002238

  264. 264.

    Bernal A.J., Pan Q., Pollack J., Rose L., Kozik A., Willits N., Luo Y., Kochetkova E., Guittet M., Michelmore R.W. Functional analysis of the plant disease resistance gene Pto using DNA shuffling. J. Biol. Chem. 2005;280:23073-23083.

    Not in our library10.1074/jbc.m500992200

  265. 265.

    Song W.Y., Pi L.Y., Wang G.L., Gardner J., Holsten T., Ronald P.C. Evolution of the rice Xa21 disease resistance gene family. Plant Cell. 1997;9:1279-1287.

    Not in our library10.1105/tpc.9.8.1279

  266. 266.
    Genes encoding pentatricopeptide repeat (PPR) proteins are not conserved in location in plant genomes and may be subject to diversifying selection · 2007
    Not checked
  267. 267.

    Gebhardt C., Valkonen J.P. Organization of genes controlling disease resistance in the potato genome. Annu. Rev. Phytopathol. 2001;39:79-102.

    Not in our library10.1146/annurev.phyto.39.1.79

  268. 268.
    Characterization of resistance gene analogues (RGAs) in apple (Malus × domestica Borkh.) and their evolutionary history of the Rosaceae family. · 2014
    Not checked
  269. 269.

    Ota T., Nei M. Divergent evolution and evolution by the birth-and-death process in the immunoglobulin VH gene family. Mol. Biol. Evol. 1994;11:469-482.

    Not in our library10.1093/oxfordjournals.molbev.a040127

  270. 270.

    Sudupak M.A., Bennetzen J.L., Hulbert S.H. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics. 1993;133:119-125.

    Not in our library10.1093/genetics/133.1.119

  271. 271.

    Bar-Hen A., Charcosset A., Bourgoin M., Guiard J. Relationship between genetic markers and morphological traits in a maize inbred line collection. Euphytica. 1995;84:145-154.

    Not in our library10.1007/bf01677953

  272. 272.

    Cao J., Schneeberger K., Ossowski S., Gunther T., Bender S., Fitz J., Koenig D., Lanz C., Stegle O., Lippert C., et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 2011;43:956-963.

    Not in our library10.1038/ng.911

  273. 273.

    Huang X., Kurata N., Wei X., Wang Z.X., Wang A., Zhao Q., Zhao Y., Liu K., Lu H., Li W., et al. A map of rice genome variation reveals the origin of cultivated rice. Nature. 2012;490:497-501.

    Not in our library10.1038/nature11532

  274. 274.
    A haplotype map of allohexaploid wheat reveals distinct patterns of selection on homoeologous genomes · 2015
    No notice
  275. 275.

    Gore M.A., Chia J.M., Elshire R.J., Ersoz E.S., Hurwitz B.L., Peiffer J.A., McMullen M.D., Sun Q., Grills G.S., Ross-Ibarra J., et al. A first-generation haplotype map of maize. Science. 2009;326:1115-1117.

    Not in our library10.1126/science.1177837

  276. 276.

    Chia J.M., Song C., Bradbury P.J., Costich D., de Leon N., Doebley J., Elshire R.J., Gaut B., Geller L., Glaubitz J.C., et al. Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 2012;44:803-807.

    Not in our library10.1038/ng.2313

  277. 277.

    Genomes Project C., Abecasis G.R., Altshuler D., Auton A., Brooks L.D., Durbin R.M., Gibbs R.A., Hurles M.E., McVean G.A. A map of human genome variation from population-scale sequencing. Nature. 2010;467:1061-1073.

    Not in our library10.1038/nature09534

  278. 278.

    Van der Linden C.G., Wouters D.C., Mihalka V., Kochieva E.Z., Smulders M.J., Vosman B. Efficient targeting of plant disease resistance loci using NBS profiling. Theor. Appl. Genet. 2004;109:384-393.

    Not in our library10.1007/s00122-004-1642-8

  279. 279.

    Gu Y., Zhao Q., Sun D., Song W. A genetic linkage map based on AFLP and NBS markers in cauliflower (Brassica oleracea var. botrytis). Bot. Stud. 2008;49:93-99.

    Not in our library

  280. 280.
    Peroxidase profiling reveals genetic linkage between peroxidase gene clusters and basal host and non-host resistance to rusts and mildew in barley. · 2010
    Not checked
  281. 281.

    Vossen J.H., Dezhsetan S., Esselink D., Arens M., Sanz M.J., Verweij W., Verzaux E., van der Linden C.G. Novel applications of motif-directed profiling to identify disease resistance genes in plants. Plant Methods. 2013;9:37.

    Not in our library10.1186/1746-4811-9-37

  282. 282.

    De Keyser E., Shu Q.Y., van Bockstaele E., de Riek J. Multipoint-likelihood maximization mapping on 4 segregating populations to achieve an integrated framework map for QTL analysis in pot azalea (Rhododendron simsii hybrids). BMC Mol. Biol. 2010;11:1-19.

    Not in our library10.1186/1471-2199-11-1

Cited by papers we hold 1

Reads

Read by people on this page

None yet.

Checked or read by AI through naulon

None yet.

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.

Are you an author?

Is this your paper?

Claim it to add your note and be paid when agents cite it. Free.